The Genes Eye View of Evolution

OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
TH E GEN E’S -E Y E VI EW

OF EVOLUTION
Praise for The Gene’s-Eye View of Evolution:

‘Arvid Ågren has undertaken the most meticulously thorough
reading of the relevant literature that I have ever encountered. And he
deploys an intelligent understanding to pull it into a coherent story.
As if that wasn’t enough, he gets it right.’ -Richard Dawkins
‘The idea of the selfish gene revolutionised evolutionary thinking
and led to many new insights. But from the outset, it received strong
criticism, not all of it baseless. In the first dedicated book on the topic,
Arvid Ågren expertly sets out the power and nuances of the selfish
gene concept. At times taking sides, at others leaving history to decide,
he is always perceptive, scholarly, balanced, and good natured.
Interwoven with asides on the principal players, this fine book suc-
ceeds in being both enlightening and engaging.’ -Andrew Bourke,
Professor of Evolutionary Biology, University of East Anglia, UK
‘Since its inception in the 1970s, the “gene’s eye view of evolution”
has been a controversial idea in evolutionary biology. In this lucid and
scholarly book, Arvid Ågren provides a masterful treatment of the
intricate and often confusing debates over the value and limitations of
the gene’s eye view. I highly recommend his book to anyone seeking
a deeper understanding of this important issue.’ -Samir Okasha,
Professor of Philosophy of Science, University of Bristol, UK
‘This book’s conversational style, clear presentation and well-
planted surprises make it ideal for both general readers and students
in a broad range of fields. The selfish gene is alive and well and con-
tinues to inspire and irritate, which is why we see gene level argu-
ments of fans and critics alike in past and present debates. Best of all,
as we follow the gene’s eye view around in Agren’s book, we find
ourselves educated about current views in exciting subfields-from
evolutionary systems theory to Major Transitions and Selfish Genetic
Elements- and rewarded with a treasure trove of references.’ -Ullica
Segerstrale, Professor of Sociology, Illinois Institute of Technology,
Chicago, USA
‘Science needs ingenious points-of-view that help us understand

the world. Few perspectives are more famous—or notorious—than
that of the selfish gene. Merging biology and history of science, Ågren
unravels its origins, explains why it is useful, and when its utility has
been overstretched. Whether you’re a fan or a critic, this is an essential
guide to the gene’s eye view.’ -Tobias Uller, Professor of Evolutionary
Biology, Department of Biology, Lund University, Sweden
TH E
GENE’S -E Y E
V I EW OF
EVOLUTION
by
J. A RV I D ÅGR E N
Wenner-Gren Fellow
Department of Organismic and
Evolutionary Biology
Harvard University
1
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For
my father, the biologist
and
my mother, the cultural historian
Preface
One of my biggest embarrassments in life is that I am such a poor

naturalist. My botanical skills are distinctly average and my ornitho-
logical knowledge is downright appalling. Rather than a love of natural
history, what attracted me to biology was a fascination with the logic
of the theory of evolution by natural selection. No other theory
explains so much with so little. It is truly deserving of the title of ‘the
single best idea anyone has ever had’, as Daniel Dennett once put it.
And in contrast with other great theories of science, like general rela-
tivity or quantum mechanics, it can be (mis-)understood by anyone.
I have always been drawn to the conceptual issues of evolutionary
biology, questions that my hard-nosed empirical colleagues would
dismiss as too theoretical, too abstract, and, if they wanted to be really
mean, too philosophical.
This is a book about one of those issues, the gene’s-eye view of
evolution.The book came about thanks to Francis Crick’s Gossip Test.
According to Crick, your true interests are revealed by what you gos-
sip about. For me, that has long been the gene’s-eye view, and the
vituperative debate that has surrounded selfish genes for the past half-
century. As this book will make clear, the story of the gene’s-eye view
deals with many abstract questions, but it also has innumerable empir-
ical implications. It strikes right at the heart of the question of what
evolution is, and how we go about studying it.
I have been thinking about the disagreements over the gene’s-eye
view for the past decade, ever since I moved to Toronto, Canada, to
begin my graduate research. Arriving in Toronto after growing up in
Sweden and receiving my undergraduate training in Scotland meant
x Pr e face
that I for the first time came in close contact with students from
North America. One thing that struck me about my new colleagues
was that they often had a very different perspective on theoretical
issues in evolutionary biology than I did. To exaggerate and overgen-
eralize a bit: if when I was a teenager and expressed an interest in the
big questions of evolutionary biology I was handed a book authored
by Richard Dawkins, they had been given one of Stephen Jay Gould’s.
I learned a tremendous amount discussing these issues in the lecture
halls, seminar rooms, and, especially, in the Graduate Student Union
pub located right next to the Department of Ecology and Evolutionary
Biology of the University of Toronto. The genesis of this book owes
a lot to those intellectual sparring sessions.
More concretely, several people were instrumental in making this
book a reality. In particular, David Haig, and his Fundamental
Interconnectedness of All Things discussion group, provided an environ-
ment that encouraged tackling the foundational questions of our field.
Few have thought more about the gene’s-eye view than David and he
has been reliable source of advice and support throughout this project.
I am grateful a large number of colleagues who took the time to read
and provide comments on my writing. For help with individual chap-
ters, I thank Alan Grafen, Alister McGrath, Andrew Bourke, Anthony
Edwards, Cédric Paternotte, Charles Goodnight, Dan Dennett, Dan
Hartl, Denis Noble, Ellen Clarke, Erik Svensson, Jack Werren, Jim
Mallett, John Durant, Jonathan Birch, Kevin Foster, Lutz Fromhage,
Megan Frederickson, Michael Bentley, Michael Rodgers, Stephen
Wright, Stu West, and Tim Lewens. Others, including David Barash,
Brian and Deborah Charlesworth, Andy Clark, James Marshall, and
Martin Nowak, answered questions and pointed me to resources that
have been tremendously helpful. For reading the entire manuscript, at
one point or another, I am indebted to Chinmay Sonawane, Cody
McCoy, David Haig, Jon Ågren, Manus Patten, Richard Dawkins, Samir
Okasha, Steve Stearns, and Tobias Uller.
Their comments greatly improved the text, clarified my thinking,
and offered much needed encouragement. On occasion, they also saved
Pr e face xi
me from some embarrassing misunderstandings. They did not always

agree with my argument; sometimes they were just kind enough to
explain why I was wrong. Any remaining mistakes are, of course, mine.
Several people helped me understand how the gene’s-eye view has
been received around the world. I am grateful for the insight from
Adrian Stencel, Amitabh Joshi, Ehud Lamm, Ian Caldas, Israt Jahan,
Jae Choe, Jun Otsuka, Kazuki Tsuji, Leonardo Campagna, Philippe
Huneman, Snait Gissis, Sakura Osamu, and Victor Luque. Only a small
portion of this topic made it into the book in the end, but I hope to
return to it in the future.
It has been said that being published by Oxford University Press is
like ‘being married to a duchess: the honour is greater than the pleas-
ure’.That has not been my experience. Ian Sherman and Charles Bath
have been extremely supportive and helpful since the first day of this
project. I am grateful to Spencer Barrett for introducing me to Ian,
and to Spencer and Locke Rowe for helping me draft the proposal.
Two chapters are partly based on material from my previously pub-
lished papers and I thank the publishers for letting me reuse some of
the text. Chapter 4 draws on Ågren JA. 2018. The Hamiltonian view
of social evolution. Studies in History and Philosophy of Biological and
Biomedical Sciences. 68–69: 88–93. Chapter 5 incorporates material
from Ågren JA. 2016. Selfish genetic elements and the gene’s-eye view
of evolution. Current Zoology. 62: 659–665 and Ågren JA and AG Clark.
2018. Selfish genetic elements. PLoS Genetics. 14: e1007700.
Throughout the time of writing I was financially supported by the
Wenner-Gren Foundations, whose generous support I am very thank-
ful for. I also indebted to the staff at the Ernst Mayr Library at the
Museum of Comparative Zoology at Harvard for their help and
assistance, especially for their ingenuity during the extraordinary cir-
cumstances of a global pandemic.
Finally, I am forever grateful to my wife, Utako, for her never-
ending love and support. And for insisting that I write this book.
J. Arvid Ågren
March 2021
Contents
Introduction: A New Way to Read Nature 1

1 Historical Origins 11
1.1 Introduction 11
1.2 Adaptationism and the legacy of natural theology 13
1.3 Population genetics 25
1.4 Levels of selection 35
1.5 Summary 45
2 Defining and Refining Selfish Genes 46
2.1 Introduction 46
2.2 What is a selfish gene? 49
2.3 Replicators and vehicles 57
2.4 Memes 64
2.5 General formulations of evolution by natural selection 68
2.6 Summary 78
3 Difficulties of The Theory 80
3.1 Introduction 80
3.2 Anthropomorphizing 82
3.3 Epistasis, heterozygote advantage, and the averaging fallacy 89
3.4 The bookkeeping objection 97
3.5 Genetic determinism 103
3.6 Human nature and human affairs 108
3.7 Summary 115
4 Inclusive Fitness and Hamilton’s Rule 116
4.1 Introduction 116
4.2 The origin and diversity of Hamilton’s Rule 120
xiv Con t e n ts
4.3 The gene’s-eye view and inclusive fitness: equivalence

or historical accident? 129
4.4 Maximization of inclusive fitness and the Formal
Darwinism Project 137
4.5 Recent reconciliations between the gene’s-eye view
and inclusive fitness 143
4.6 Summary 149
5 Empirical Implications 151
5.1 Introduction 151
5.2 Extended phenotypes 153
5.3 Greenbeards 159
5.4 Selfish genetic elements 164
5.5 Summary 178
Conclusion: The Gene’s-Eye View Today 180
Why should biologists study the history of ideas? 181
Metaphors and mathematics 185
Die, selfish gene, die? 188
The gene’s-eye view worldwide 190
Final thoughts 193
References 195
Index235
Introduction: A New Way

to Read Nature
T here really is something special about biology. The French bio-

chemist and Nobel Prize winner Jacques Monod described its
position among the sciences as simultaneously marginal and central
(Monod 1970, p. xi). It is marginal, because its object of study—living
organisms—are but a special case of chemistry and physics, contribut-
ing to only a minuscule part of the universe. Biology will never be the
source of natural laws in the way physics is. At the same time, if, as
Monod believed, the whole point of science is to understand human-
ity’s place in the world, then biology is the most central of them all.
No other field of study deals so directly with the question of who we
are and how we got here in the first place.
The location of biology among the sciences means that its theories
can never be just theories. They will always touch us in a deeper way
than those in other subjects. This is especially true for the theory
of evolution. On one level, it is simply a theory of how different rates
in sex and death lead to different configurations of carbon molecules.
On another, it is our story of creation. How we think about the the-
ory of evolution therefore matters more than the way we think about
other scientific theories.
The gene’s-eye view is one way to think about evolution. In its
original formulation, Charles Darwin’s theory of evolution by natural
selection was a theory about individual organisms. Individuals vary in
The Gene’s-Eye View of Evolution. J. Arvid Ågren, Oxford University Press. © J. Arvid Ågren 2021.
DOI: 10.1093/oso/9780198862260.003.0001
2 T h e Ge n e’s-Ey e V i ew of Evolut ion
heritable traits, and if any of them make the individual more likely to
survive and reproduce, these traits will become more common in the
population as the generations go by. T he gene’s-eye view represents a
subtle but radical shift in perspective. Building on the insight from
population genetics that evolutionary change can be described as the
increase or decrease of certain genetic variants, it argues that evolu-
tion is best thought of from the perspective of genes. By this reason-
ing, organisms are nothing but temporary occurrences—present in
one generation, gone in the next. And, as a consequence, organisms
cannot be the ultimate beneficiary in evolutionary explanations.
Instead, this role is filled by the gene. Genes are considered immor-
tal and they pass on their intact structure from generation to gener
ation. This way of thinking is also called selfish gene thinking, because
natural selection is conceptualized as a struggle between genes, usually
through the effects they have on organisms, for replication and trans-
mission to the next generation. Here, ‘genes’ is used in a somewhat lax
way. The evolutionary struggle is not between different genes within
the same organism (though, as will become clear, the gene’s-eye view
offers a powerful way to think about such genetic conflicts) but
between different alleles of the same gene within a population.
The origin of the gene’s-eye view involved many people, but two
stand above the rest: the American George C. Williams (1926–2010)
and the Brit Richard Dawkins (1941–). The idea was first explicitly
laid out by Williams in Adaptation and Natural Selection (Williams 1966),
and then 10 years later more forcefully by Dawkins in The Selfish Gene
(Dawkins 1976). Few phrases in science have caught the imagination
of laypeople and professionals alike the way that ‘selfish gene’ has
done, and it changed how both groups thought about evolution and
natural selection. Among both groups, the gene’s-eye view, has subse-
quently amassed both strong supporters and fierce critics.
The debate over the value of the gene’s-eye view has raged for over
half a century. It has pitted 20th century Darwinian aristocrats such as
John Maynard Smith and W.D. Hamilton against Richard Lewontin
and Stephen Jay Gould in the pages of Nature as well as those of The
I n t roduct ion: A n ew way to r e a d natu r e 3
New York Review of Books. Even today, commentators cannot agree. For
example, in 2015 when the science historian Nathaniel Comfort
reviewed the second volume of Dawkins’s autobiography for Nature he
referred to the gene’s-eye view as ‘looking increasingly like a twentieth-
century construct’ (Comfort 2015). In contrast, writing for the same
journal only a few months later, the biologist turned journalist and
businessman Matt Ridley concluded that ‘no other explanation [for
evolution] makes sense’ (Ridley 2016). Professional biologists remain
equally divided. Simon Conway Morris dismissed it as ‘an exploded
concept that was almost past its sell-by date as soon as it was popular-
ized’ (Conway Morris 2008, p. ix). Similarly, a senior colleague of mine
who I showed an early draft of this manuscript wondered if he really
would be a suitable person to provide feedback as he disagreed with
‘virtually every aspect of the field’ and as a result he has ‘trouble separat-
ing their bad science from good faith attempts to describe it’. Yet,
Andy Gardner called The Selfish Gene ‘unequivocally the most
important popular book on evolutionary biology of the 20th century’
(Gardner 2016), a view shared by the Royal Society who in July 2017
announced that, after a public poll, The Selfish Gene had been voted
‘the most inspiring science book of all time’.
Much of the discomfort over the gene’s-eye view comes from its sur-
rounding vocabulary. Genes are ‘selfish’, organisms mere ‘survival
machines’, and bodies nothing but ‘lumbering robots’. T he philosopher
Roger Scruton complained that these ideas made ‘cynicism respectable
and degeneracy chic’ (Scruton 2017, p. 49). Along these lines, a com-
monly told story (meaning it is seemingly impossible to track down
the original source) is that The Selfish Gene was the favourite book of
the disgraced Enron CEO Jeffrey Skilling, and that he used the book
to justify the exploitative cutthroat culture of the company.
But the debate over the gene’s-eye view is about so much more.
It overthrows our conception of familiar biological terms like gene,
fitness, and organism. It brings to the forefront evolutionary biologists’
peculiar habit of speaking of biological entities as having intentions,
deploying strategies, and pursuing goals. It drills to the core of what
we mean by causality in evolutionary explanations. T he gene’s-eye

view has featured in many major debates in evolutionary biology over
the past half century, including in technical disagreements over epista-
sis, heterozygote advantage, and inclusive fitness, and in public discus-
sions over what it means to be human. T his book is about all of that.
How to think like a selfish gene
The gene’s-eye view occupies a peculiar position within theoretical

biology. In his review of The Selfish Gene, W.D. Hamilton called it a
‘new way to read nature’ (Hamilton 1977). What does that mean?
The gene’s-eye view is not a concrete empirical hypothesis (though it
certainly helps us come up with such) and it is not an all-encompassing
mathematical framework (though general models can be constructed).
Instead, it is a way to make sense of the biological world. Dawkins
once described it as: ‘a particular way of looking at animals and plants,
and a particular way of wondering why they do the things they do’
(Dawkins 1982a, p. 1). Put like that, one can easily see why it would
be difficult to come up with experiments that would reject it. This
could be viewed as a strength or as a weakness. Take for example, one
of the most quoted passages from The Selfish Gene:
Now they [genes] swarm in huge colonies, safe inside gigantic lum-
bering robots, sealed off from the outside world, communicating with it
by tortuous indirect routes, manipulating it by remote control. T
hey are
in you and in me; they created us, body and mind; and their preservation
is the ultimate rationale for our existence. (Dawkins 1976, p. 25)
Dawkins’s statement contains the essence of the gene’s-eye view:

while Earth is inhabited by organisms, what ultimately matters for
evolution is the propagation of genes, a process that genes play an
active part in. The gene’s-eye view prompts us to look at biological
phenomena and ask cui bono? Who benefits? (Dennett 1995, p. 325).
The perspective treats adaptations as the central problem of evolu-
tionary biology and argues that it is only by understanding that genes,
not organisms or groups, are the ultimate beneficiaries of natural

selection that they can be understood.
As Denis Noble has pointed out, however, this notion is unfalsifia-
ble. The only empirical content of the above statement is that genes
are located inside organisms (Noble 2006, pp. 12–13). Noble rewrites
the statement, removing what he considers to be unsubstantiated
speculation:
Now they [genes] are trapped in huge colonies, locked inside highly
intelligent beings, moulded by the outside world, communicating with
it by complex processes, through which, blindly, as if by magic, func-
tion emerges. T hey are in you and me; we are the system that allows
their code to be read; and their preservation is totally dependent on
the joy we experience in reproducing ourselves. We are the ultimate
rational for their existence. (Noble 2006, pp. 12–13).
In Noble’s version the organism is in control; genes are passive prison-

ers. There is no clear cut empirical data or ingenious mathematical
model that can distinguish Noble’s version from Dawkins’s.
To make sense of disagreements like this, Ullica Segerstrale has sug-
gested that the right way to approach the gene’s-eye view is with a logical
rather than a literal mind (Segerstrale 2000, p. 261). By a logical mind, she
meant that the gene’s-eye view grew out of an intellectual environment
where it was common to design, often quite elaborate, thought experi-
ments to explore how evolution works. In the preface of The Selfish Gene,
Dawkins makes this point explicitly when he describes the book as being
‘designed to appeal to the imagination’ (Dawkins 1976, p. xi). Segerstrale
contrasts such a logical environment with the literal intellectual milieu
that tends to characterize experimental and molecular biologists. Here,
the focus is less on exploring possible theoretical scenarios and more on
carefully describing the features of the biological system at hand. Someone
trained in the logical tradition will have no problem asking themselves ‘if
I was a gene, what would I do in this situation?’, whereas a biologist from
a literal background will find the question absurd.
The emphasis on the logic of evolution and natural selection shares
many features with how philosophers do their work. Segerstrale
argues—as do Sterelny (2001, pp. 4–6), Ruse (2003, p. 164), and Noble
(2006, p. 11)—that this philosophical approach to evolution is more
common among British biologists than among their colleagues from
other countries. This may at first seem strange, as it has been said of
the British that they do not do philosophy. For example, Ernst Mayr
complained about ‘illiterate Anglo-Saxons’ who had not read enough
Hegel (Kohn 2004, p. 329), and Iris Murdoch described the picture of
the world painted by English philosophers as one in ‘in which people
play cricket, cook cakes, make simple decisions, remember their child-
hood and go to the circus’ (Murdoch 1953, p. 35). T he debate over the
gene’s-eye view shows why Mayr and Murdoch were being unfair.
Disagreements over the value of the ideas in Adaptation and Natural
Selection and The Selfish Gene raised the bar for conceptual discussions
of biological phenomena considerably and were instrumental in the
emergence of the philosophy of biology as a distinct field of study.
This book is about how to think like a selfish gene. Darwin once
described the term ‘natural selection’ as ‘in some respects a bad one, as it
seems to imply conscious choice; but this will be disregarded after a little
familiarity’ (Darwin 1868, p. 6; my emphasis). My goal is to provide a little
familiarity to the gene’s-eye view: what it is, where it came from, how it
changed, and why it still evokes such strong emotions. In so doing, I will
argue that the gene’s-eye view is one of the most powerful heuristics
or thinking tools there is in biology. Like all tools, however, to get the
most out of it you must understand what task it what designed to solve.
Aims and outline of the book
I have written the book I wish already existed. There was no book-
length treatment of the history and current state of the gene’s-eye
view. Instead, anyone looking for a systematic summary of the topic
has typically had to scramble together papers and chapters from m
ultiple
sources. Furthermore, much of the debate about the value of the
gene’s-eye view and its role in modern evolutionary theory has been
conducted in the philosophical literature, which has meant that many

biologists are unaware of the many nuances of the case for and against
selfish genes. T
hough things are improving, especially in evolutionary
biology, it would be going too far to say that the attitude often attrib-
uted to Richard Feynman that ‘philosophy of science is as useful to
scientists as ornithology is to birds’ has completely disappeared.
This books aims to teach the controversy. T he term ‘teach the con-
troversy’ has a bad reputation among evolutionary biologists, and for
good reason. For the past decades it has been the cornerstone of the
strategy applied by the Discovery Institute to discredit the status of
evolutionary theory and to promote the teaching of intelligent design
in American public schools. It played a key role in the Kitzmiller vs
Dover Area School District trial of 2005, which ruled that intelligent
design ‘cannot uncouple itself from its creationist, and thus religious,
antecedents’, meaning that its teaching violated the constitutionally
mandated separation of church and state. It is therefore ironic that the
term was originally coined by a self-described secular liberal professor
of English, Gerald Graff, with the aim of showing students that aca-
demic knowledge is the product of a dynamic process with disagree-
ments that are settled through empirical observations and deductive
reasoning (see Graff 1992). Personally, I have always enjoyed popular
accounts of scholarly debates, whether about string theory in The
Trouble with Physics (Smolin 2006) and Not Even Wrong (Woit 2006), or
the role of mathematical modelling in economics and physics in
Economic Rules (Rodrik 2015) and Lost in Math (Hossenfelder 2018), and
I carefully followed the debate about participant–observer ethnog
raphy in the aftermath of the publication of On the Run (Goffman 2014).
Learning the controversy is a thrilling way to be introduced to a new
field and this book is written in that original Graffian spirit.
The book spans five core chapters. In Chapter 1, I outline the his-
torical origins of the gene’s-eye view. I argue that its intellectual core
stands on three legs. The first is the tradition that takes adaptation, the
appearance of design in the living world, as the central problem that
the theory of evolution must answer. T his view of the field has been
particularly prominent in the United Kingdom and I trace this back

to the historically strong standing of natural theology in the country.
The second leg is the emergence of population genetics during the
development of the Modern Synthesis. J.B.S. Haldane, Sewall Wright,
and R.A. Fisher all showed how evolution can be mathematically
captured as a change in allele frequencies, which moved the attention
of biologists from organisms to genes. I will argue that Fisher was
especially important and that he introduced a novel conception of the
environment fundamental to the gene’s-eye view. T he final leg is the
levels of selection debate. This is the debate over whether natural
selection can act on levels above or below the individual organism. In
particular, both Williams and Dawkins identified the widespread, and
in their view misguided, popularity of group selection as providing
the direct impetus to write their books.
Both Adaptation and Natural Selection and The Selfish Gene received
a lot attention upon publication and the ensuing debate quickly
resulted in a rather confusing vocabulary. In Chapter 2, I describe how
the gene’s-eye view uses familiar terms in unfamiliar ways. Most
important of these terms is ‘gene’ itself, which is used in a rather
abstract way, agnostic about any molecular details. I also outline how
the gene’s-eye view matured in light of the criticism it received and
how the abstract use of the term gene was integral to one of the
gene’s-eye view’s most fundamental claims: that evolution requires
two entities, replicators and vehicles. I discuss how this formulation of
selection and evolution fares relative to other general accounts, such
as Lewontin’s principles, and how this relationship has changed in
light of the growing interests in the major transitions. Finally, I evalu-
ate the concept of memetics, the application of the gene’s-eye view to
cultural evolution and outline why it has failed to have the same
influence there as it has on the study of organic evolution.
In Chapter 3, I tackle some of the most common criticisms of the
gene’s-eye view. I first discuss the use of intentional language and the
anthropomorphizing involved in calling genes selfish. I show how this
habit has greatly annoyed critics within biology and beyond, and that
this debate is the most recent instantiation of the old conflict over
whether teleological explanations have a place in biology. Next, I outline
the criticisms that came from mathematical population geneticists.
I revisit the classic cases of epistasis and heterozygous advantage to
evaluate how the gene’s-eye view handles interactions between genes,
and whether it is bound to commit the so-called averaging fallacy.
I also discuss the charge from developmental biologists that the gene’s-
eye view affords unwarranted amounts of causal power to genes in the
process of development and in so doing ignores too many other inter-
esting biological processes. Lastly in this chapter I deal with how the
gene’s-eye view fits into evolutionary biology’s troubled relationship
with the concept of human nature and morality. This is a debate that
raged intensely in the early days of the gene’s-eye view but which has
by now largely calmed down. Nevertheless, I show how a close read-
ing of the views of Williams and Dawkins on these issues reveals
interesting parallels with those of T.H. Huxley.
Chapter 4 examines the long and intimate association between the
gene’s-eye view and the work of W.D. Hamilton. Hamilton was cru-
cial to the emergence of the gene’s-eye view, especially through his
work on inclusive fitness and what is now known as Hamilton’s Rule.
Hamilton’s key insight was that individual organisms can affect the
transmission of their genes not only through personal reproductive
success but also through the success of close relatives. Inclusive fitness
provides a way to view this process from the perspective of the indi-
vidual organism, but it can also be seen from a gene’s-eye view.
Dawkins and others have repeatedly emphasized the formal equiva-
lence of the two perspectives.Yet, as I will argue in this chapter, there
is an under-appreciated potential tension between the two. I demon-
strate how this tension shows up in both the disagreements over the
value of inclusive fitness theory stemming from Nowak et al. (2010)
and in Alan Grafen’s ongoing Formal Darwinism Project. I end the
chapter by discussing two recent attempts to resolve this tension.
The gene’s-eye view initially earned its stripes by helping the field
make crucial strides in the study of old problems in evolutionary biology,
in particular related to social behaviour. It also helped launch new

avenues of empirical research. Chapter 5 is dedicated to three such
new areas. The first is extended phenotypes, which are examples of
phenotypic effects that occur outside of the body in which the gene
is located. The second area is greenbeard genes, which gets its name
from the thought-experiment devised to show that for altruism to
evolve it is the relatedness between the actor and the recipient at the
locus underlying the altruistic behaviour that matters, not the genome-
wide relatedness. Finally, selfish genetic elements are genetic elements
that have the ability to promote their own transmission even if it
comes at the expense of the fitness of the individual organism. I dis-
cuss the state of the current understanding of these phenomena and
the role of the gene’s-eye view in uncovering them. I also show how
all three examples add ammunition to the gene’s-eye view’s attempt
to undermine the centrality of the individual organism in evolution-
ary explanations by demonstrating how individual organisms may fail
to maximize their own fitness.
The book is primarily aimed at graduate students in biology, upper
year undergraduates, and others seeking an introduction to the gene’s-
eye view of evolution. I also hope that it will be useful to more senior
people in evolutionary biology and neighbouring fields looking for a
fresh perspective on a familiar debate, as well as to philosophers and
historians of biology who are interested in how biologists view this
part of their recent history. Any primer struggles to find the balance
between being cohesive and being comprehensive. In writing this
book, I have had two aims: firstly to produce a book that would be
cohesive enough to offer a one-stop introduction to the many debates
surrounding the gene’s-eye view, and secondly to make it compre-
hensive enough to show just how vast and nuanced these debates have
become and to provide a road map to anyone who wants to go on and
further explore this rich literature on their own.
1
Historical Origins
1.1 Introduction
S everal books and papers were crucial for the emergence of the
gene’s-eye view, but it culminated with the arrival of The Selfish
Gene in the fall of 1976. The exact timing of the book’s publication
owes much to two defining conflicts of modern British history. T he
first was the industrial conflict between the UK National Union of
Mineworkers and Edward Heath’s Conservative government. In the
1970s, coal burning was responsible for the majority of British elec-
tricity production, and strike action by coal miners had led to serious
power shortages. The situation climaxed on New Year’s Day 1974
when the government introduced the so- called ‘three-
day week’.
One consequence of the lack of power was that Richard Dawkins,
then a young lecturer who had recently returned to Oxford after a
stint as Assistant Professor at the University of California at Berkeley,
stopped his research on cricket behaviour and turned to writing.
When the conflict was over, and power returned to normal, one
chapter was complete. It lay forgotten in a drawer until a sabbatical in
1975, which Dawkins spent at home in Oxford writing the next chap-
ters of the book in a ‘frenzy of creative energy’ (Dawkins 2016, p. xiii).
The other was the Battle of Trafalgar. Michael Rodgers, the Oxford
University Press editor who would eventually acquire the book, was
first told about the project by the physicist Roger Elliott, one of
Dawkins’s colleagues at New College, Oxford, and then later came
DOI: 10.1093/oso/9780198862260.003.0002
across it in an internal memo that reported a conversation between

the head of the Academic Division at the Press, Dan Davin, and the
philosopher Anthony Quinton who had mentioned that ‘a New
College man was writing a rather lively book on the function of the
gene’ (Rodgers 2017). Having read the first few chapters, Rodgers is
said to have rung Dawkins, booming down the telephone ‘I must have
that book!’ (Dawkins 2013a, p. 276). The Selfish Gene was published on
28 October 1976, having been delayed one week to avoid clashing
with the release of The Oxford Companion to Ships and the Sea. In the
UK, 21 October is Trafalgar Day, which celebrates the Royal Navy’s
victory over Spain and France at the Battle of Trafalgar in 1805 and,
on recommendation of W.H. Smith booksellers, naval books were
given priority (M. Rodgers, personal communication).
Dawkins has repeatedly emphasized the debt that the views presented
in The Selfish Gene owed to other biologists, in particular R.A. Fisher,
John Maynard Smith, Robert Trivers, W.D. Hamilton, and George
Williams. He asked Trivers to write the foreword to the book, described
Fisher and Hamilton as the leading candidates for the title ‘most
distinguished Darwinian since Darwin’ (Dawkins 2000) and said

that the most important thing for a successful conference was that
Maynard Smith would attend and that the venue have ‘a large and
convivial bar’ (Dawkins 1993a). After The Selfish Gene, Williams’s
Adaptation and Natural Selection is the most important book in the
gene’s-eye view’s origins story. In his foreword to the 2019 edition of
that book, originally published 10 years before The Selfish Gene,
Dawkins describes it as the most important book in evolutionary
biology of the second half of the 20th century, on par with the ‘canon’
of the 1930s and 1940s, and that it was the only book that he would
insist that all his students read during his time as an Oxford tutor
(Dawkins 2019).
This chapter traces the history of the gene’s-eye, arguing that three
areas provided the intellectual foundation: adaptationism, population
genetics, and the levels of selection debate. Adaptationism is the
tradition that takes the appearance of design in the living world as the
cardinal problem that a theory of evolution must be able to explain.
H istor ica l or igi ns 13
This tradition has been especially important in British biology and its
through that intellectual milieu that the gene’s-eye view emerged.
The gene’s-eye view treats adaptation as a special kind of problem that
deserves a special kind of explanation. Key advocates of the gene’s-eye
view have often invoked the writings of the theologian William Paley,
the author of Natural Theology (Paley 1802), to make this point and
I therefore begin the chapter by outlining the strong standing of natural
theology in the country and how that legacy transitioned into an
adaptationism that remains to this day.
The population genetics of the modern synthesis in the 1930s put
genes at the centre of evolutionary explanations. T he new mathemat
ical approach of population genetics had brought together the
particulate inheritance of Mendel with the gradualism of Darwin.
J.B.S. Haldane, Sewall Wright, and R.A. Fisher in their own ways for-
mally characterized the process of evolution as one of changes in the
frequency of allelic variants. They did not use the agential language of
the modern gene’s-eye view, but their work provided the foundations
on which this approach was built. I will argue that this was especially
true of the work of Fisher and that his definition of the environment
only really makes sense from a gene’s-eye view.
The last area was the levels of selection debate and specifically the
rejection of group selection as an explanation for social behaviour.
Both Williams and Dawkins pointed directly at the popularity of
group selection arguments as the stimulus to write their own books.
Furthermore, Williams’s insistence on parsimony, that biologists
should not appeal to selection at higher levels than necessary, com-
bined with W.D. Hamilton’s theory of inclusive fitness, led to a rapid
change in opinion regarding how to think about adaptation.
1.2 Adaptationism and the legacy

of natural theology
The biological tradition of adaptationism owes much to the field of

natural theology. As an area of inquiry, natural theology is based on the
assumption that the study of the natural world allows inferences to be

made about the divine world. Natural theology has a long history and
has been practiced in multiple faith traditions. The English approach
to natural theology that came to play such an important role in the
emergence of evolutionary theory was a product of particular time and
place (see Alister McGrath’s Darwinism and the Divine (McGrath 2011)
for an extensive history). It came to prominence in conjunction with
another quintessential English institution, the Anglican Church, and it
played a central role in the Church’s efforts to smooth tensions among
various Protestant factions that were at odds on both theological and
political issues.
Natural theology also provided a way to institutionalize the rise of
science. The 19th century Oxford mathematician Baden Powell noted
that the Reformation’s emphasis of removing the authority of the
Church led to a ‘peculiarly Protestant prejudice’ of constantly seeking
evidence and proof for faith (quoted in McGrath 2011, p. 56). T he
empirical study of nature, including natural history, neatly slipped into
this niche and it allowed new scientific results to be interpreted within
the framework of the Church. This is not to suggest that views on the
relationship between science and faith among British Protestants were
completely homogeneous, instead extensive variation existed among
the various denominations, as well as emerging agnostics and atheists
(Stanley 2015). Nonetheless, the Church’s attitude would later on lead
to the rise of the scientifically literate country vicar—a profession
Darwin himself aspired to when he arrived at Cambridge as an
undergraduate—who could combine his church duties with a passion
for natural history.
The importance of the Anglican tradition for strengthening natural
theology’s bond to English biology can also be seen by contrasting the
English approach to that of Protestants in other parts of Europe
(Ruse 2003, 2018). T ake, for example, Immanuel Kant whose Lutheran
Pietist upbringing gave him a deeply rooted scepticism of reason and
science as a route to salvation. T hat scepticism was shared among
many contemporary Protestants, who considered natural theology
a distraction from the strict emphasis on the direct access to God for
ordinary people, not just philosophers and other learned people.
Rejecting natural theology did not mean Kant was sceptical of modern
science. In contrast, he was deeply impressed by Newtonian physics;
to him it just had nothing to contribute to matters of faith.
1.2.1 Why William Paley matters

The profile of natural theology in England was raised through a
number of public events. For example, the Boyle Lectures (delivered
1692–1732) were set up with the aim of providing a ‘confutation
of atheism’ and ‘proving the Christian Religion against notorious
Infidels’. The lectures were a popular attempt by the Church of
England to stem the rising tide of scepticism. No person, however, is
more associated with the English approach to natural theology than
the theologian William Paley. Born in Peterborough, England, in 1743
he graduated from Christ’s College, Cambridge as Senior Wrangler,
the university’s top undergraduate student in mathematics, in 1763.
He would go on to become a fellow of the college, where he gave
lectures on moral philosophy. The book that emerged from these
lectures, Principles of Moral and Political Philosophy (Paley 1785), was
hugely influential. It quickly became a set text for students at
Cambridge and featured in many defining debates, including in the
early days of the newly formed United States Congress.
Paley’s last book would become even more famous. Having already
written several books on Christian apologetics, none reached the
heights of Natural Theology or, Evidences of the Existence and Attributes of
the Deity, Collected from the Appearances of Nature, published 3 years
before his death (Paley 1802). It was a huge popular success and
remained in print for over a century, going through over 50 editions
in the UK alone. There was very little new intellectual work in Natural
Theology. Instead, it is largely restating arguments that had been devel-
oped by others during the 17th and 18th century. There is even a
good case to be made that Paley plagiarized parts of the book. In
particular, Paley relied extensively on the work of the Dutchman

Barnard Nieuwentyt, including the use of the watch analogy (LeMahieu
1976, pp. 60–61). Paley also ignored the serious critiques of natural
theology that had been developed by then, including those by David
Hume and Immanuel Kant.
Instead of intellectual novelty, it was Paley’s fluent and convincing
writing, coupled with a deft use of verbal imagery, that made the
book stand out. The opening paragraph of Natural Theology is a case in
point and it lays out his core argument in a few powerful sentences:
In crossing a heath, suppose I pitched my foot against a stone and were

asked how the stone came to be there, I might possibly answer that for
anything I knew to the contrary it had lain there forever; nor would it,
perhaps, be very easy to show the absurdity of this answer. But suppose
I found a watch upon the ground, and it should be inquired how the
watch happened to be in that place, I should hardly think of the answer
which I had given, that for anything I knew the watch might have
always been there.Yet why should not this answer serve for the watch
as well as for the stone; why is it not admissible in that second case as
in the first? For this reason, and for no other, namely, that when we
come to inspect the watch, we perceive—what we could not discover
in the stone—that its several parts are framed and put together for
a purpose, e.g., that they are so formed and adjusted as to produce
motion, and that motion so regulated as to point out the hour of the
day; that if the different parts had been differently shaped from what
they are, or placed in any other manner or in any other order than that
in which they are placed, either no motion at all would have carried
on in the machine, or none which would have answered the use that
is now served by it. (Paley 1802, p. 7)
Gardner (2009) describes how Paley’s conception of design stands on

two legs: contrivance and relation. Contrivance refers to how the
constituent parts of both watches and organisms appear as if contrived
for a specific purpose. Relation, in turn, captures how the parts
demonstrate a unity of purpose, they are all working towards the
same goal. On Paley’s heath, this is what distinguishes the watch from
the stone.
Just as early Anglican natural theologians were successful partly

because they provided a stabilizing force in the aftermath of the
English Civil War (1642–1651) and the Glorious Revolution (1688), so
did Paley in his time. Natural Theology appeared in the midst of the
European turmoil associated with the aftermath of the French
Revolution. France, England’s old neighbour and rival, was ruled by a
threatening Napoleon and was seeing the rise of atheistic views. For
example, when asked about the role of God in describing the cosmos,
the astronomer Pierre-Simon Laplace is said to have replied: ‘Je n’avais
pas besoin de cette hypothèse-là’ (I had no need of that hypothesis). In
England, the writings of Paley provided a counterweight to this
attitude, reinforcing the idea that science could be done within the
embrace of the established Church. In particular, he showed how the
image of a mechanistic universe subject to natural laws established
by Newton and his followers could strengthen belief rather than
undermine it (though, Paley thought that astronomy, owing to its
‘simplicity’, had little to offer as evidence of the Creator; Paley 1802,
p. 199).
Ultimately, Natural Theology was about strengthening the case for
God. Given the time when it was written it was therefore no
coincidence that he chose to build his case on machines and organisms.
It is a book primarily about animals. Plants do get a chapter but are
dismissed as unimportant: ‘it is unnecessary to dwell upon a weaker
argument, where a stronger is at hand’, as he put it (Paley 1802, p. 183).
Paley wrote in the middle of the Industrial Revolution and his readers
would have been well acquainted with the watches, telescopes,
stocking- mills, and steam engines that feature in his argument
(Gillespie 1990). ‘That an animal is a machine’, Paley wrote, ‘is a
proposition neither correctly true nor wholly false’ (Paley 1802, p. 48).
Both machines and organisms are examples of contrivances and can
therefore only be understood by understanding the intentions of their
designer. To illustrate this, Paley provided an extensive discussion of
the intricate mechanisms of a telescope in order to drill home the
importance of complexity for his argument (Paley 1802, pp. 16–31).
He then points out that a human eye is far more complicated than a
telescope and the eye therefore requires a more sophisticated designer.
1.2.2 Neo-Paleyan biology in Britain

Paley represented the apogee of the English approach to natural
theology, especially its popular variety. Later on, the Bridgewater
Treatises were commissioned by Francis Henry Egerton, 8th Earl
of Bridgewater, and published from 1833 to 1840 with the goal of
showing ‘the Power, Wisdom, and Goodness of God, as manifested in
the Creation’.
Today, few similar initiatives remain. One prominent exception is
the Gifford Lectures, put on every year by the ancient Scottish uni-
versities (St Andrews, Glasgow, Aberdeen, and Edinburgh). Organized
for the first time in 1888, the stated aim of the lectures is to ‘promote
and diffuse the study of natural theology in the widest sense of the
term – in other words, the knowledge of God’. Presenting the lectures
remains a prestigious honour in Scottish academia, and several distin-
guished contemporary theologians interested in science have given
them, such as Alvin Plantinga (2004–2005) and Alister McGrath
(2009). In recent years the scope of lectures seems to have strayed
from the original goal. For example, several prominent atheists have
also been invited, including Carl Sagan (1985), Richard Dawkins
(1988), Michael Ruse (2001), Steven Pinker (2012–2013), and Sean
Carroll (2016).
The strong standing of natural theology has meant that relative to
their colleagues in other countries British biologists have been
preoccupied with life’s design-like qualities. Already a few decades
after the publication of Natural Theology, the collections at the Oxford
University Museum of Natural History were organized by chapter
orders of the book, with the stated aim of familiarizing students with
Paley’s argument (McGrath 2011, p. 134). Recently, this adaptationist
tendency in Britain has been characterized by Tim Lewens as ‘Neo-
Paleyan’ (Lewens 2019a).
When Darwin entered Christ’s College, Cambridge, to prepare for

the priesthood after dropping out of his medical studies at the
University of Edinburgh, Paley was very much on the agenda. Not
only because Darwin had joined Paley’s old college (legend even has
it that they occupied the same room), but because Paley’s Views of the
Evidences of Christianity (Paley 1794) was required reading. Alongside
with Natural Theology it left a deep impression on Darwin who would
later write:
I am convinced that I could have written out the whole of the

Evidences with perfect correctness, but not of course in the clear
language of Paley. The logic of this book and, as I may add, of his
Natural Theology gave me as much delight as did Euclid. (. . .) I did
not at that time trouble myself about Paley’s premises; and taking
these on trust, I was charmed and convinced by the long line of argu-
mentation. (Darwin 1887, p. 47)
Similarly, short after the publication of the Origin, Darwin wrote in a

letter to his friend John Lubbock: ‘I do not think I ever admired a
book more than Paley’s Natural Theology: I could almost formerly
have said it by heart’ (Darwin Correspondence Project 2020a). In
addition to quotes like these, the influence of Paley also shines through
in the way Darwin constructs his arguments, as both Gould (2002,
pp. 118–121) and McGrath (2011, pp. 156–157), have highlighted. Most
importantly, both Paley and Darwin start with a human object or
activity that would be familiar to the reader: a watch or telescope for
Paley and breeding of farm animals in the case of Darwin. They then
proceed to point out the similarities to their own proposed mechanism.
Both also spend considerable time on the human eye, either to
highlight its extrinsic contrivance or to demonstrate how a gradual
selective process can produce the same result. In his influential history
of biology, The Growth of Biological Though, Ernst Mayr argues that the
fact that most biologists of Darwin’s time were natural theologians, in
practice studying what we today would refer to as adaptations, meant
that most of the natural theology literature could be folded into the
new field of evolutionary biology in a rather frictionless way

(Mayr 1982, pp. 104–105; see also Reiss 2011, pp. 122–124).
A final example of Paley’s influence is the title of Darwin’s book
on the co-evolution between pollinators and orchids, On the Various
Contrivances by which British and Foreign Orchids are Fertilised by Insects
(Darwin 1862), published only 3 years after The Origin of Species. Even
at that time, ‘contrivance’ was a term strongly associated with natural
theology and with Paley. T o Darwin, natural selection was clearly the
answer to the problem of design, as formulated by Paley. Moreover,
when Darwin submitted the book to his publisher John Murray he
wrote that ‘like a Bridge-water Treatise the chief object [of the book]
is to show the perfection of the many contrivances of orchids’ (Darwin
Correspondence Project 2020b). Similarly to how Dawkins would
later praise Natural Theology for its excellent documentation of
complex adaptations ( just with the wrong conclusions drawn from
the data), Darwin’s book was lauded in venues like the Literary
Churchman that it could have been read as a contribution to natural
theology ( just with the wrong conclusion drawn from the data). T he
botanist Asa Gray went so far as to say that: ‘if the Orchid book (with
a few trifling omissions) had appeared before the “Origin”, the author
would have been canonized rather than anathematised by the natural
theologians’ (quoted in McGrath 2011, p. 157).
Darwin’s attitude to Paley and natural theology was in sharp con-
trast to that of his biggest supporter, T.H. Huxley. While Darwin’s
establishment background had meant that he had been exposed to the
Anglican natural theology consensus since a young age, Huxley’s
more modest upbringing came with no such training. Michael Ruse
has speculated that this is why Huxley remained so unimpressed with
the concept of adaptation (Ruse 2019a).
Someone who was impressed by adaptations was R.A. Fisher. Fisher
was not only an accomplished statistician and population geneticist,
but also a deeply committed Anglican. At Cambridge, he regularly
gave sermons at the college chapel and wrote essays for church maga-
zines. (He also spent many years at the godless University College
London, which to this day lacks a divinity department.) In a letter to

Darwin’s granddaughter, the botanist and geneticist Nora Barlow, he
admits feeling guilty for never actually finishing Natural Theology
(Bennett 1983, p. 79). Nevertheless, Fisher considered adaptation to be
the defining feature of the living world and evidence of God’s
continued involvement:
To the traditionally religious man, the essential novelty introduced by
the theory of evolution of organic life, is that creation was not all finished
a long time ago, but is still in progress, in the midst of its incredible
duration. In the language of Genesis we are living in the sixth day,
probably rather early in the morning and the divine artist have not yet
stood back from this work and declared it to be ‘very good’.
(Fisher 1947)
Paley shines through also in the writings of the next generation of

British evolutionary biologists. They may not have read Paley directly
but that did not prevent them from invoking his name for rhetorical
purposes. One who did read Paley was Vero Copner Wynne-Edwards,
author of Animal Dispersion in Relation to Social Behaviour (Wynne-
Edwards 1962) and often assigned the role of representative of naive
group selection in the current literature. Paley is said to have influenced
Wynne-Edwards’s concept of the ‘balance of nature’ and his ideas
about how animals can regulate their own population size towards an
optimum number that prevents the overexploitation of their resources
(Borello 2010, p. 42).
The influence of Paley is even more vividly demonstrated by
the attitude of two of modern British evolutionary biology’s most
eloquent spokesmen, John Maynard Smith and Richard Dawkins.
Maynard Smith credited reading Darwin for his loss of faith and he
had no hesitation regarding what he considered the central problem
of evolutionary biology to be:‘the main task of any theory of evolution
is to explain adaptive complexity, i.e. to explain the same set of facts
which the eighteenth-century theologian Paley used as evidence of a
Creator’ (Maynard Smith 1969, p.82). This opinion is very much
shared by Dawkins. He has described the zoology department at
Oxford that he joined as a student a strongly adaptationist (Dawkins

2015a, pp. 342–345), much thanks to the domineering presence of
E.B. Ford, author of the influential Ecological Genetics (Ford 1964). In
contrast, continental Europeans and Americans have considered the
origin and constraint on diversity the central problem for evolution
to explain (Sterelny 2001, pp. 4–6; Lewens 2004, p. 21). T his is of course
somewhat of an exaggeration, but much has been written about this
strong standing of adaptationism in the UK, most extensively by
Marek Kohn in A Reason For Everything (Kohn 2004).
Given that adaptationism, especially as represented by the Ford legacy
at Oxford, was dismissed by Richard Lewontin as stemming from the
‘fascination with birds and gardens, butterflies and snails that was charac-
teristic of the pre-war upper middle class from which so many British
scientists came’ (Lewontin 1972), it is ironic that for long its best articula-
tion was Arthur Cain’s 1964 paper ‘The perfection of animals’ (Cain 1964).
Cain’s humble upbringing background was far from upper-middle class.
At the 1979 Royal Society meeting on ‘The Evolution of Adaptation by
Natural Selection’ organized by John Maynard Smith, Cain gave one of
the responses to Stephen Jay Gould’s talk (a talk that would eventually
become the famous Spandrels of San Marco paper; Gould and
Lewontin 1979), in which he remarked that: ‘Presumably when preju-
dice is strong, facts can be dispensed with as well: my own background
and upbringing could only be distinguished by the extreme purist from
working class’ (retold in Dawkins 2015a, p. 344).
After admitting that other candidates, such as the species problem
or the origin of biological diversity left him cold, Dawkins argues that
adaptive complexity is a unique kind of problem that deserves a
unique kind of scientific explanation: either a Designer, as invoked by
Paley, or something like natural selection (Dawkins 1998a). By now,
Dawkins may be as famous for his public defence of atheism, as he is
for his work in evolutionary biology (Giberson and Artigas 2007,
pp. 19–52). His attitude to the Scottish philosopher David Hume
is therefore quite informative and reveals the close bond he feels
with Paley. Hume’s Dialogues Concerning Natural Religion, published
anonymously 3 years after his death, is often considered to be one of

the best refutations of the design argument (Hume 1779). In the
Dialogues, three philosophers, Philo, Demea, and Cleanthes, debate the
evidence for the existence of God, in particular the argument from
design. At one point, Philo, who is believed to represent Hume’s own
view, argues that the evidence of design can be used to support a wide
range of mutually exclusive conclusions. Even that:
This world was only the first rough attempt of some infant god, who
afterwards abandoned it, ashamed of his poor performance; it is the
work of some dependent, inferior god, whose superiors hold it up for
ridicule; it was produced by some god in his old age and near-senility,
and ever since his death the world has continued without further
guidance, activated by the first shove he gave to it and the active force
that he built into it. (Hume 1779, p. 26)
To Dawkins, this misses the point. He is deeply impressed with the

evidence of design and only disagrees with Paley regarding the origin
of design. In his 1986 book The Blind Watchmaker (which for the
American market was given the subtitle ‘Why the Evidence of
Evolution Reveals a Universe without Design’). Dawkins describe
Paley as having ‘a proper reverence for the complexity of the living
world, and he saw that it demands a very special kind of explanation’
(Dawkins 1986a, p. 4; my emphasis). It is this belief that led Dawkins
to describe himself as a ‘neo-Paleyist obsessed with the illusion of
purpose, adaptation’ (Dawkins 1994a; ‘Paley, of course, was a paleo-
Paleyist’, he adds) or ‘transformed Paleyist’ (Dawkins 1998a, p. 16). It is
also why Dawkins argues that it was only after Darwin, that it became
possible to be an intellectually fulfilled atheist (Dawkins 1986a, p. 6).
His point was that the weakness of the design argument had been
noted before, but in the absence of a credible alternative the design
argument was never mortally wounded.
As documented by Lewens (2019a), the rhetoric of Paley remains
also in contemporary British evolutionary biology. The best repre-
sentatives of this habit are the theoreticians Andy Gardner and Alan
Grafen. In a 2009 paper entitled ‘Adaptation as organism design’, which

on his website he describe as his ‘manifesto’, Gardner writes, explicitly
acknowledging, Paley’s contributions: ‘The problem of adaptation is to
explain the apparent design of organisms. Darwin solved this problem
with the theory of natural selection’ (Gardner 2009). Similar language
is used by Grafen when describing the rationale for his Formal
Darwinism Project: ‘Adaptation is the centre of biology, adaptation is
design, and maximising fitness is what organisms are designed for’
(Grafen 2007). In both cases, Gardner and Grafen do not shy away
from the word design but instead fully embrace it as integral to what
adaptation is. The issue whether evolutionary biology actually needs
a design principle—an answer to the question of what organisms should
appear designed to maximize—comes up in the current debate over
inclusive fitness and I will return to that issue when discussing the
relationship between the gene’s-eye view and inclusive fitness, including
the Formal Darwinism Project, in Chapter 4. For now, it suffices to say
that the problem of design occupies a special place in British evolution-
ary biology, a place that it does not occupy in other national traditions.
It is worth noting a clear exception to this generalization, the
American George Williams. Early on in Adaptation and Natural
Selection,Williams describe adaptation as a ‘special and onerous concept
that should not be used unnecessarily, and an effect should not be
called a function unless it is clearly produced by design and not by
chance’ (Williams 1966, p. 5) and then goes on to state that the book
is ‘an attack on what I consider unwarranted uses of the concept of
adaptation’ (Williams 1966, p. 11; see also Williams 1985). Like Dawkins
and Maynard Smith, Williams thought that adaptation was a unique
problem, and in the last chapter of the book he extensively quotes
Paley’s comments about the human eye to justify this. He even
introduces the term teleonomy (cf. Pittendrigh 1958) as the term to
describe the study of adaptation, a term subsequently endorsed by
Dawkins (1982a, p. 81).Williams also included excerpts from chapters 1
and 3 of Paley’s Natural Theology as an appendix in his last book Natural
Selection: Domains, Levels and Challenges (Williams 1992).
Taken together, the gene’s-eye view owes to natural theology in

general, and to Paley in particular, its view of adaptive complexity, the
appearance of design in the living world, as the problem that a theory
of evolution needs to be able to address.
1.3 Population genetics
William Provine’s landmark history of the field describes theoretical

population genetics as the product of a clash of two different per-
spectives on evolution (Provine 1971). In one corner was Darwin’s
original formulation, which emphasized how natural selection acted
on small continuous variations leading to gradual evolutionary
change. In the other were those who thought that selection on small
variants would not be enough to generate large-scale evolutionary
change. This conflict intensified with the rediscovery of Mendel’s
work in 1900. Darwin’s ideas were especially vulnerable to the attack
that the Mendelian concept of particulate genetic changes was
incompatible with his own theory, as he had lacked a functioning
theory of inheritance of his own. The formulation of population
genetics resolved the disagreement. The key works were all pub-
lished in an intense decade and a half between 1918 and 1932 by the
Britons R.A. Fisher and J.B.S. Haldane, and the American Sewall
Wright.
Fisher, Haldane, and Wright all contributed both to the reconcilia-
tion of Darwin and Mendel and to the introduction of theoretical
population genetics as it is known it today. They all championed a
new mathematical way of doing biology, an approach that was not
appreciated by everyone. Ernst Mayr, for example, famously ques-
tioned the value of their contributions: ‘What, precisely, has been the
contribution of the [Fisher, Wright, and Haldane] mathematical
school to evolutionary thinking? If I may be permitted to ask such a
provocative question’ (Mayr 1959). Mayr coined the term ‘beanbag
genetics’ to describe their approach, resulting in Haldane’s spirited
‘A defense of beanbag genetics’ the following year (Haldane 1964).

The exact views of Fisher, Wright, and Haldane, however, differed
quite markedly. Provine described the relationship between their
views as ‘symmetrical’, in the sense that each of them thought the
other two had more in common (Provine 1971, p. 176). T hey disagreed
on issues such as the importance of dominance, epistasis, drift, and
whether selection would be more efficient in large or small populations.
Who of the three got most things right is a popular debate at happy
hour among graduate students in evolutionary biology and in the
more sober reflections of professional historians of science. I will
argue, however, that if we restrict ourselves to the gene’s-eye view,
Fisher towers above the other two.
The intellectual foundations of the gene’s-eye view can in retrospect
be said to be implicit in the writings of Haldane and Wright, but to
be explicit in the writings of Fisher (Sarkar 1994; Okasha 2008a;
Ewens 2011; Edwards 2014). I will therefore focus on the views of
Fisher and especially on how his major contribution, the Fundamental
Theorem of Natural Selection, opened up the avenue to think in
terms of a gene’s-eye view.
1.3.1 Ronald Aylmer Fisher

The mathematical talents of R.A. Fisher were recognized early. Already
as a seven-year-old he attended lectures by the Irish astronomer and
celebrated popularizer of science Sir Robert Ball and these talents
would later be nurtured as a boarder at Harrow School. Fisher
famously suffered from a greatly reduced eyesight, which meant that
he was not allowed to work under direct electrical light. His tutors at
Harrow therefore had to teach him mathematics without visual aids
and without pen and paper. It is said that this left him with an unusual
mathematical intuition and an ability to solve mathematical problems
in his head. This ability has also been suggested to be the reason why
many of us with lesser mathematical minds struggle with the many
mathematical intuitive leaps that characterize Fisher’s writing. Indeed,
as pointed out by Alan Grafen: ‘if your understanding of [Fisher’s

Fundamental Theorem of Natural Selection] comes from reading
Fisher himself, you should be aware that virtually no other biologists
have understood what he meant’ (Grafen 2003). Fisher left Harrow
for Gonville and Caius College, Cambridge in 1909. Like Paley, he
was a Wrangler in the Mathematical Tripos, achieving the honour in
1912. His fascination with biology began before arriving in Cambridge.
As reported by his daughter Joan Fisher Box, he brought with him to
Cambridge a thirteen-volume set of the complete works of Darwin
(a school prize; Fisher Box 178, p. 17). While there, his interest in evo-
lution was further spurred by reading Karl Pearson’s collection of
papers Mathematical Contributions to the Theory of Evolution. Pearson
was from the generation before Fisher’s and his interest in mathematical
statistics, of which he is widely considered one of the founding fathers,
and evolutionary theory in the form of biometry (as well as eugenics)
meant that he left a strong impression on the young Fisher. Later, the
two of them would both have offices in the same building at the
University College London. Personal and scientific disagreements,
however, would eventually lead to the two of them falling out.
1.3.2 Fisher (1918) and the birth of the gene’s-eye view

If you were to put a date on the origin of the gene’s-eye view, Fisher’s
graduate student A.W.F. Edwards has suggested 1 October 1918
(Edwards 2014). This was the publication date of Fisher’s ‘The correl
ation between relatives on the supposition of Mendelian inheritance’
in the Transactions of the Royal Society of Edinburgh. Fisher had initially
submitted the paper to the Royal Society of London, but unfavour
able reviews from among others R.C. Punnett (of Punnett squares)
and Karl Pearson prevented publication. T he machinations behind the
rejection also included G.H. Hardy (of the Hardy–Weinberg equilib-
rium; see Norton and Pearson 1976 for the full story). Like much of
Fisher’s writing, the 1918 paper is a tough read, but it is worth the slog.
As suggested by the title, Fisher’s goal is to examine correlations in
traits between relatives in light of Mendelian inheritance (a topic pre-

viously addressed by Pearson who reached different conclusions,
hence his negative reaction).
The contributions of the paper were many (Moran and Smith 1966).
In particular, Fisher calculated the expected values of the correlation
between relatives under a variety of scenarios, including linkage,
partial recessivity, epistasis, and assortative mating. T
o do this, Fisher
developed the statistical method of regressing genotypic value on the
number of alleles at a given locus (0, 1, or 2 in a diploid), which also
led to the introduction of the term variance.
The concept of variance is key to understanding why the 1918
paper can be thought to be the birth of the gene’s-eye view. Edwards
(2014) explains it as follows. Consider a locus with genotypes AA, Aa,
and aa. Their genotypic values are i, j, and k and are present in the
population with frequencies P, 2Q, and R respectively. Now, using a
least-square regression approach we can calculate the regression coef-
ficient, α, of the genotypic value given the number of A alleles, such
that:
P (Q + R )(i - j ) + R(P + Q )( j - k )
a=
P (Q + R ) + R(P + Q )
The regression coefficient, α, is the expected change in the genotypic

value for a given substitution, i.e. going from aa to Aa, or Aa to AA.
With this in place, Fisher’s genetic variance, the part that he calls the
‘additive part which reflects the genetic nature without distortion’,
can be written as:
(P + R )a 2 - (Pa - Ra )2
Fisher contrasts this additive genetic part with a residue part ‘which
acts in much the same way as an arbitrary error introduced into the
measurements’. This, then, is the crux: any variation not included in
the variance captured by the linear regression should not be considered
genetic but instead be thought of as random environmental noise.
This may seem like a subtle point, but here Fisher introduces a
radically expanded notion of the environment. The expanded notion
of environment is awkward from the perspective of individual organism
but makes sense under a gene’s-eye view.
From a gene’s-eye view, or more precisely from the perspective of
an allele, Fisher’s notion has the consequence that in a diploid
organism, the other allele present at the same location in the genome
should be considered part of the environment. And so should all other
genes in the genome, as well as all the other genes in the population
(the gene pool). This idea of the genomic environment is key to
appreciating the deep connection between Fisher’s Fundamental
Theorem and the gene’s-eye view. It also highlights how the gene’s-
eye view could more accurately be called the allele’s-eye view.
Fisher expanded on these ideas in his 1922 paper ‘On the dominance
ratio’, also in a journal run by the Royal Society of Edinburgh
(Fisher 1922). This paper included, among other things, the first
demonstration of the consequences of heterozygote advantage, a

phenomenon that later would be used by Elliott Sober and Richard
Lewontin as an argument against the gene’s-eye view. I will return to
this topic in Chapter 3. In the succeeding years, Fisher focused on
applying his theoretical models to empirical data and worked on
issues like genetic variation in British moths (Fisher and Ford 1926)
and mimicry (Fisher 1927). In 1930, he synthesized his ideas his
most famous publication, The Genetical Theory of Natural Selection
(Fisher 1930).
1.3.3 The Genetical Theory of Natural Selection

Julian Huxley called The Genetical Theory of Natural Selection ‘the most
important book to have come out this century’ (quoted on the jacket
of the 1999 Oxford University Press Variorum Edition). Almost a
century later many would still agree and the book ranks among the
most important of the modern synthesis. Other than the mathematical
sections, the manuscript was typed by his wife, Eileen, mostly in the
evenings and weekends, as Fisher spent his weekdays as Head of

the Statistics Department at Rothamsted Experimental Station. In
retrospect, Fisher would write that the chief goal of the book was to
confront the claim that ‘the discovery of Mendel’s laws of inheritance
was unfavourable, or even fatal, to the theory of natural selection’
(Fisher 1954). Spanning twelve chapters it opens with a Preface that
begins with the famous sentence: ‘Natural Selection is not Evolution’.
Arguably the most important part of the book, at least for our purposes
here, is Chapter 2 where he introduces the Fundamental Theorem of
Natural Selection.
If The Genetical Theory is still highly regarded, the Fundamental
Theorem of Natural Selection, has a more mixed legacy. That Fisher
himself thought highly of the Fundamental Theorem is implied not
only by its grand name but also by his likening it to the second law of
thermodynamics (Fisher 1930, p. 36) and his description of it as
occupying ‘the supreme position among the biological sciences’
(Fisher 1930, p. 37). In contrast, the attitude of most evolutionary
biologists of subsequent generations has been lukewarm, if not directly
hostile. The mathematician Sam Karlin is often attributed the
comment (though usually without reference, for example, Walsh and
Lynch 2018, p. 154) that the Fundamental Theorem is ‘neither
fundamental nor a theorem’, which was the consensus position among
theoretical population geneticists up until at least the mid 1990s. At
that time, a number of authors used George Price’s 1972 paper to
reinterpret the Fundamental Theorem, reinstating some of the
importance Fisher had awarded it (Price 1972; Edwards 1994;
Grafen 2003; Queller 2017). The disagreements between what has
been called the traditional and modern interpretations of the
Fundamental Theorem continue to this day (see, e.g., the exchange
between Grafen 2018 and Lessard and Ewens 2019 for contrasting
views).
Here, I am less concerned with taking sides about the mathematical
correctness or biological significance of the Fundamental Theorem, but
rather with evaluating its connection to the gene’s-eye view. To do
so, however, requires us to unpack the assumptions of the theorem

and to derive the origin of the traditional and modern interpretations.
1.3.4 The gene’s-eye view and the Fundamental

Theorem made clear
Early on in The Genetical Theory, Fisher defined the Fundamental
Theorem as: ‘The rate of increase in fitness of any organism at any
time is equal to its genetic variance in fitness at that time’ (Fisher 1930,
p. 35). One look at this original definition quickly provides some
insight why it has been marred by misunderstandings and disagree-
ments. What does genetic variation in fitness of an organism even
mean? Later on in Chapter 2, Fisher used ‘species’ instead of ‘organ-
ism’ and in 1941 replaced it with ‘population’. In 1941, he also added
the qualification ‘ascribable to a change in gene frequency’. Both
changes help clarify that Fisher’s central claim is that the rate at which
natural selection increases the average fitness of a population through
changes in gene frequencies will be equal to the genetic variation in
fitness at the time (Box 1.1).
The traditional attitude that the Fundamental Theorem mostly fails
lasted until 1989 when A.W.F. Edwards published a paper in Theoretical
Population Biology bringing attention to a long-neglected 1972 paper
by the brilliant and troubled American George Price (see Harman 2011
for a gripping biography). Price’s ‘Fisher’s “fundamental theorem”
made clear’ spans only twelve pages, but its influence on changing
attitudes towards the Fundamental Theorem was immense. Grafen
(2003) described it as the ‘path of enlightenment towards the
fundamental theorem’. As discussed above, no one should feel bad if
they struggle to understand Fisher. Price (1972) put it thus: ‘Fisher’s
explanations of his theorem are afflicted by a truly astonishing number
of obscurities, infelicities of expression, typographical errors, omissions
of crucial explanations, and contradictions between different passages
about the same point’ (Price 1972). The key point that Price made
clear about the Fundamental Theorem was that what Fisher was
Box 1.1. Unpacking the Fundamental Theorem

The Fundamental Theorem can be divided into two key concepts
(Okasha 2008a). T he first is simply the average fitness of a population.
If we define fitness of the i th individual as wi then we can write the
å
n
wi
average fitness of a population of size n as w = i
. The change in
n
the average fitness over time can then written either as dw in a
dt
continuous model (as Fisher originally did) or, following Ewens
(1989), as Dw for a discrete time model (the discrete time steps can,
e.g., be from one generation to the next).
The second concept, the genetic variance in fitness, takes a little
longer to unpack. I will largely follow Okasha’s (2008a) terminology,
including his slightly simplified version of what Fisher called the
‘average effect’ further down.
Fisher’s unusual mathematical intuitions have made many of us
struggle with his arguments. It is well established that variation
in fitness can be due to genetic differences among individuals,
environmental variation, or a combination of the two. The way
Fisher talks about ‘genetic variance’ can therefore be confusing. He
does not refer to the total variation in fitness due to differences in
genotype between individuals, Var( g ), but instead to what we now
typically refer to as additive genetic variance. Additive genetic variance,
Varadd ( g ) , is only part of the total genetic variance, with the non-
additive (sometimes called epistatic, which also includes dominance)
variance, Varnon-add ( g ) , making up the other part, such that:
Var( g ) = Varadd ( g ) + Varnon-add ( g )
Additive genetic variance (Fisher’s ‘genetic variance’) captures

how a gene affects fitness, independently of what other genes are
present in the genome. To see what this means, imagine the extreme
case where there are no interactions between genes and that they
all act completely independently of each other. In this scenario,
the total genetic variance will equal the additive variance, that is
Var ( g ) = Varadd ( g ) . Now, using Fisher’s (1918) regression method
described above, the fitness of a diploid individual, i, can be

written as:
wi =åa j xij + ei
j
Recall, that α was defined earlier in the chapter as the regression

coefficient of fitness on the number of copies of a given allele so that
xij is the number of j alleles carried by individual i. a j thus tells us
how much the fitness of an individual changes if you were to add
one more copy of the j allele (assuming the rest of the genome stays
the same). This is what Fisher called the ‘average effect’. ei is the
residual term and under perfect additivity it would be 0 and wi would
equal åa x .
j
j ij
The additive genetic variance, Varadd ( g ) , is then equal to:
Var åa j xij .
j
Under the traditional interpretation of the Fundamental Theorem,

Fisher’s was thought to have argued that the change in the average
dw ö
fitness over time æç ÷ would equal the additive genetic variance,
è dt ø
Var ( g ) (or Varadd ( g ) in the discrete-time model). In both cases,
add
w
this seems to mean that the average fitness of a population will never
decrease.
If this indeed what Fisher meant, it is easy to see why so many people
have been sceptical. There are many ways fitness may decrease in a
population, even if it is subject to natural selection and the change in
average fitness of the population will thus not be equal to the additive
genetic variance (as a variance cannot be negative).
concerned with was not the total change in average fitness of a popu-
lation, but the part of the total change that is due to natural selection
changing gene frequencies in a constant environment.
Price’s insight about the constant environment is key. Recall that
Fisher introduced a radically broad definition of environment that
included all the genes in the genome, as well as the population’s gene
pool, when he developed the regression method to determine an
allele’s average effect. Fisher’s idea of a constant environment meant
that the average effect of all alleles stays the same from one generation
to the next. Thus, if the average effect of one allele has changed, the
environment is considered to have changed. Price’s insight about
the constant environment also reveals the deep connection between
the Fundamental Theorem and the gene’s-eye view. Grouping biotic
environmental effects (what biologists usually mean by the word)
with non-additive genetic effects, such as dominance and epistasis as
parts of the environment, only really makes sense under a gene’s-eye
view (but see Sober 2020 for a pushback against this conclusion).
The importance of this conception of the environment runs
through most Dawkins’s writings. For example, in the foreword to the
30th anniversary edition of The Selfish Gene he writes:
Each gene [is] pursuing its own self-interested agenda against the
background of the other genes in the gene pool—the set of candidates
for sexual shuffling within species. Those other genes are part of the
environment in which each survives, in the same way was the weather,
predators and prey, supporting vegetation and soil bacteria are part of
the environment. From each gene’s point of view, the ‘background’
genes are those with which it shares bodies in its journey down the
generation. In the short term, that means the other members of the
genome. In the long term, it means the other genes in the gene pool of
the species. Natural selection therefore sees to it that gangs of mutually
compatible—which is almost to say cooperating—genes are favoured
in the presence of each other. (Dawkins 2006a, pp. xii–xiii)
The idea of a genomic environment is even more clearly laid out in

the chapter titled ‘The selfish cooperator’ in Unweaving the Rainbow
where he writes:
At each genetic locus, the gene most likely to be favoured is the one
that is compatible with the genetic climate afforded by the others, the
one that survives in that climate through repeated generations. Since
this applies to each one of the genes that constitute the climate—since
every gene is potentially part of the climate of every other—the result

is that a species gene pool tends to coalesce into a gang of mutually
compatible partners. (Dawkins 1998b, p. 215)
In both quotes, the influence of Fisher shines through. Indeed, Michael

Wade would later criticize The Selfish Gene by saying that Dawkins
argument would have worked ‘[i]f evolution in natural populations
followed the paradigm developed by R. A. Fisher’ (Wade 1978). In his
original formulation, Dawkins made this argument using the analogy
of a rowing crew. I will return to this when discussing the epistasis and
the so-called averaging fallacy in Chapter 3.
Finally, whether we accept Fisher’s expanded notion of environ-
ment will also determine our attitude to the biological significance of
the Fundamental Theorem. Although, Price (1972) was instrumental
in shifting attitudes towards the mathematical correctness of the
Theorem, he described Fisher’s idea of treating non-additive gene
effects as environment as a ‘defect’ of the Theorem (Price 1972, p. 139).
According to Price, this defect meant that the environment is always
changing and that we can therefore not actually say anything about
whether mean fitness will increase or decrease. The Theorem can
only make such a prediction in a constant environment. On the other
hand, from a gene’s-eye view Fisher’s expanded environment is not a
mere mathematical trick, with no biological or theoretical justification,
but the logical consequence of the shift of perspective from organism
to gene. T aking a gene’s-eye view therefore makes it easier to accept
the biological significance of the Fundamental Theorem.
1.4 Levels of selection
The third strand of evolutionary thought that the gene’s-eye view

owes its existence to is the levels of selection debate of the 1960s
and 1970s. T
hough once dismissed as a ‘rather foolish controversy’
(Waddington 1975), disagreements over which level in the biological
hierarchy—genes, organisms, groups, species—natural selection occurs

later developed into one of the liveliest areas of evolutionary biology
and indeed ‘one of the brightest areas in recent philosophy of science’
(Dennett 1995, p. 327). An important reason for the longevity of the
issue is that the debate involves both conceptual and empirical elements.
Group selection is the idea that group-level adaptations are the
product of selection not on individuals but on groups. Because group
selection can act in the opposite direction of selection at the individual
level, it can provide a mechanism for the evolution of altruism, social
behaviours that come with a fitness cost to the individual performing
them but with a benefit to the recipient and/or the group as a whole.
While theoreticians today agree that formal and proper models of
group selection can be formulated, the situation in the past century
was rather different, and talk about how individuals behaved ‘for the
good of the group’ and in order to preserve the existence of the spe-
cies was rampant.
The contentious history of group selection has been extensively
reviewed, and I will therefore provide only a brief sketch here. Anyone
looking for a longer version has several books to explore. Do note,
however, that they often arrive at diametrically different conclusions
regarding the value of group selection (it has even been difficult to
agree whether Darwin himself used group selection arguments;
Ruse 1980; Borello 2005; Gardner 2011). T o get a sense of the full
spectrum of opinion on group selection, compare the very critical
The Ant and the Peacock (Cronin 1991) and the much more positive
Unto Others (Sober and Wilson 1998) or Evolutionary Restraints
(Borello 2010). More recently, Michael Wade has provided a lovely
personal account of much of this history in Adaptation in Metapopulations
(Wade 2016). Several anthologies with key papers of the general levels
of selection debate exist (examples include Brandon and Burian 1984
and Keller 1999). Anyone looking for a guide to the many conceptual
issues related to group selection controversy, and the broader levels of
selection debate, can do no better than to consult Samir Okasha’s
Evolution and the Levels of Selection (Okasha 2006).
1.4.1 Wynne-Edwards and the origins

of naive group selection
Borello (2005) has characterized the first half of the 20th century as a
‘period of mutual acceptance, or at least benign neglect’ when it came
to the group selection question. Fisher, Haldane, and Wright all touched
on it in one way or another in their writings. Fisher allowed it some
role in the maintenance of sexual reproduction but also argued that the
fact that individuals reproduce faster than groups means that selection
on individuals will usually overpower that on groups (Fisher 1930,
pp. 122–123). Furthermore, in an essay titled ‘Some hopes of a eugeni-
cist’, he also outlined a kin selection argument for how nephews may
‘genetically’ replace a childless uncle (Fisher 1914). Haldane is famous
for the quip that ‘he was prepared to lay down his life for eight cousins
or two brothers’, a story recounted by John Maynard Smith in his
review of E.O. Wilson’s Sociobiology (Maynard Smith 1975), an idea that
he explored in Haldane (1955). In The Causes of Evolution, Haldane also
discussed examples of traits that are advantageous for a group but
harmful for the individual (Haldane 1932, p. 119). Wright appears to
have been most sympathetic towards group selection and a version of
it can be said to be part of his shifting balance theory (Wright 1931).
However, he did not discuss it in the context of social behaviour. As
usual there was thus some variation in their views, but group selection
was not a key point of contention among them.
The period of mutual acceptance came to an abrupt end in 1962.
The publication of Vero Copner Wynne-Edwards’s Animal Dispersion in
Relation to Social Behaviour kicked off the group selection debate as it is
known it today. Wynne-Edwards was not the first person to argue in
favour of group selection. Consider, for example, this section from the
conclusion of the influential 1949 textbook Principles of Animal Ecology:
The probability of survival of individual living things, or of popula-
tions, increases with the degree to which they harmonically adjust
themselves to each other and the environment. This principle is basic
to the concept of the balance of nature, orders the subject of matter of
ecology and evolution, underlies organismic and developmental biology,

and is the foundation for all sociology. (Allee et al. 1949, p. 729)
Nevertheless, Wynne-Edwards, who read zoology at New College,

Oxford, where he was briefly tutored by Julian Huxley, has been the
name most strongly associated with group selection. Across 23 chapters
and 653 pages, Animal Dispersion is one long argument that selection
on individuals is not enough to explain social behaviour. In particular,
Wynne- Edwards was concerned with how animals are prevented
from overexploiting their resources—what he referred to as ‘the
balance of nature’. He argued that animals had evolved the ability to
infer the size of their population and then regulate it accordingly to
avoid the population crashing from lack of resources. T oday, this is a
position that even the strongest proponents of modern group selection
theory call ‘naive’ (e.g. Wilson and Wilson 2007).
Wynne-Edwards’s proposal would set off a flurry of counterargu-
ments. One of the first salvos came from Wynne-Edwards’s nemesis
David Lack. Lack had published The Natural Regulation of Animal
Numbers in 1954, a book that had touched on similar topics as Animal
Dispersion (Lack 1954). Lack came down heavily on side of individual
selection, which had prompted Wynne-Edwards to write his own
book. In his 1966 Population Studies of Birds, Lack reiterated many of
the same arguments before dedicating a full appendix just to Wynne-
Edward’s book (Lack 1966). The same year another heavy blow to the
reputation of group selection would land: the publication of Adaptation
and Natural Selection by George C. Williams.
1.4.2 George Christopher Williams and Adaptation

and Natural Selection
George Christopher Williams was born in Charlotte, North Carolina,
United States in 1926 and grew up in New York and Maryland. He
did military service in Italy during World War II, working on water
purification. He subsequently enrolled at University of California at
Berkeley, where he was taught by the botanist and modern synthesis

architect G. Ledyard Stebbins. In 1955, he obtained his PhD from the
University of California, Los Angeles. Following appointments at the
University of Chicago and Michigan State University, he was recruited
to the State University of New York at Stony Brook, where he spent
the remainder of his career, playing a key role in building up the
department to be one of premier centres for evolutionary biology in
the world.
In addition to his work on the levels of selection, he made numerous
contributions to evolutionary theory (Futuyma and Stearns 2010;
Stearns 2011). For example, his 1957 Evolution paper ‘Pleiotropy, natural
selection, and the evolution of senescence’ introduced the idea of
antagonistic pleiotropy, where an allele has a positive fitness effect
early in the life cycle and a negative one later on, as an explanation for
ageing (Williams 1957). Together with Randolph Nesse, he also
founded the field of evolutionary medicine (Nesse and Williams 1994).
In 1999, he shared the Crafoord Prize in Biological Sciences from the
Royal Swedish Academy of Sciences with Ernst Mayr and John
Maynard Smith for their ‘pioneering contributions to broadening,
deepening and refining our understanding of biological evolution and
related phenomena’. He passed away in 2010 following a period of
Alzheimer’s disease.
Alongside The Selfish Gene, Williams’s Adaptation and Natural
Selection is the defining text of the gene’s-eye view. Williams’s book
was directed towards professional biologists rather than the general
public and is therefore less known than The Selfish Gene. Its influence
on the academic field of evolutionary biology, however, has been
enormous and it remains lauded by both critics (e.g. Sober and
Wilson 2011) and admirers (e.g. Boomsma 2016).
In the preface of the 30th anniversary edition of the book,Williams
recounts his motivations for writing it (Williams 1996a, p. ix). He was
spending the 1954–55 academic year at the University of Chicago on
a teaching fellowship. Chicago at the time was the home of people
like W.C. Allee and A.E. Emerson and was a stronghold for group
selection (Borello 2010). One particular day, Emerson gave a lecture

on what he had dubbed ‘beneficial death’, that individuals would
sacrifice their own lives for the benefit of the group. So distraught
with the message of the talk, Williams told his wife, the biologist
Doris Williams, that if such a presentation was ‘acceptable biology,
[he] would prefer another calling’. Later on, Williams would even go
so far as to say that if what Emerson was talking was consider sound
biology, he would be better off selling insurance (Williams 1996b).
Similarly, Dawkins has also singled out popular books on group
selection, such as Konrad Lorenz’s On Aggression (Lorenz 1963 in
original German, English translation 1966) and Robert Ardrey’s The
Social Contract (Ardrey 1970), as providing the impetus to write his
own book: ‘to undo the damage done by Ardrey and Lorenz—and by
many television documentaries of the time’ (Dawkins 2013a, p. 261).
1.4.3 Three mistakes of naive group selection

Bentley (2020) has identified three key assumptions that the early
naive group selectionists were mistaken about. The first assumption
was that group selection was required for social behaviour that comes
with a cost to the individual performing it to evolve. As Wynne-
Edwards put it:
when the short-term advantage of the individual undermines the

future safety of the race, group-selection is bound to win, because the
race will suffer and decline, and be supplanted by another in which
antisocial advancement of the individual is more rigidly inhibited.
(Wynne-Edwards 1962, p. 20)
W.D. Hamilton showed that the idea that if selection at the individual

level was favouring selfish behaviour, group selection will overpower
it was false (Hamilton 1963, 1964a, 1964b). I will explore the details of
Hamilton’s ideas regarding social evolution, including the modern
understanding of inclusive fitness and Hamilton’s Rule and how they
relate to the gene’s-eye view, in Chapter 4. For now, it is enough to
note that at he demonstrated that costly social behaviours can evolve

by individual level selection if it is preferentially directed towards
relatives.
The second assumption was that group selection as Wynne-Edwards
imagined it would be a strong selective force. In 1963, Nature published
a brief note by Wynne-Edwards, very much a précis of the book
(Wynne-Edwards 1963), which prompted John Maynard Smith to
respond in this same venue (Maynard Smith 1964). Maynard Smith’s
reply is memorable for two reasons. To start, relying on Hamilton
(1963), he coined the term kin selection to describe Hamilton’s
insight. Next, he introduced his own very influential haystack model
of group selection. In his model Maynard Smith imagines a species of
mouse that lives in haystacks spread across a meadow. Each year, mice
colonize each haystack. Once there, the mice and their offspring
reproduce throughout the summer until the harvest begins and the
mice disperse into the meadow. Next year, new haystacks are colonized
by mice that survived the previous year. The mice come in two
phenotypes: timid and aggressive. T
he aggressive mice outcompete the
timid mice within a haystack, resulting in only aggressive individuals
present at the end of the summer. However, a haystack made up of
only timid individuals will produce more individuals than do hay-
stacks with aggressive mice present. While this difference provides a
way for group selection to operate, Maynard Smith showed that when
there is migration between the haystacks, this will quickly lead to a
scenario where the aggressive mice win out. The main take-home
message of the haystack model is therefore that group selection will
usually be a weak force in nature. It is not ‘bound to win’ as Wynne-
Edwards had put it (Wynne-Edwards 1962, p. 18).
The final mistaken assumption was that group adaptations were
common in nature. This is one that Williams forcefully went after in
Adaptation and Natural Selection. Rather being the product of group
selection, he argued, many, if not most, putative examples of group
adaptation were actually examples of individual level adaptations. T
he
subtitle of Adaptation and Natural Selection was ‘A critique of some
current evolutionary thought’ and early on Williams describes the

book as ‘an attack on what I consider unwarranted uses of the concept
of adaptation’ (Williams 1966, p. 11). As discussed above, Williams
thought of adaptation as ‘a special and onerous concept’ and, to
him, the most important function of the book was to call for the
development of ‘an effective set of principles for dealing with the
general phenomenon of biological adaptation’ (Williams 1966, p. 19).
The book was relentless in its demands for clarity regarding concepts
like adaptation, selection, and fitness and it raised the standard of
argument in evolutionary biology considerably.
Williams took particular aim at the confusion between group
adaptations and ‘fortuitous group benefits’. On this,Williams’s writing
is so clear that little can be added:
Benefits to groups can arise as statistical summations of the effects of

individual adaptations.When a deer successfully escapes from a bear by
running away, we can attribute its success to a long ancestral period of
selection for fleetness. Its fleetness is responsible for its having a low
probability of death from bear attack. T he same factor repeated again
and again in the herd means not only that it is a herd of fleet deer, but also
that it is a fleet herd. T
he group therefore has a low rate of mortality
from bear attack. When every individual in the herd flees from a bear,
the result is effective protection of the herd. (Williams 1966, p. 16)
In other words, a herd of fleet deer is not the same as a fleet herd of deer.
Just because a trait is good for the group, it does not mean it evolved by
group selection. Selection on each individual deer for its running speed
may lead to the fortuitous benefit of a fast running group. In general,
Williams argued that, in the name of parsimony, biologists should not
appeal to selection at higher levels than necessary.
Williams had an incredible influence on biologists’ attitudes towards
group selection. He noted that while he was confident that his views
would eventually be considered orthodox, he was surprised how
quickly they became so. Indeed, the shift in attitude among evolu-
tionary biologists towards group selection turned out to be u nusually
rapid. Geoffrey Parker would later say that in order to get published
in 1965 you had to be a group selectionist, whereas 10 years later you

had to be a kin selectionist (quoted in Segerstrale 2000, p. 54).
In general, the study of social behaviour in the 1960s and 1970s was
buzzing with new theoretical advances. In addition to Hamilton,
Maynard Smith, and Williams, Robert Trivers had a large influence
through his papers on reciprocal altruism (Trivers 1971) and on
parent–offspring conflict (Trivers 1974). R.A. Fisher (Fisher 1958) and
Richard Lewontin (Lewontin 1961) had introduced game theory as a
theoretical framework to evolutionary biology, and this approach
reached a larger audience with the publication of Maynard Smith and
Price’s ‘The logic of animal conflict’ in Nature in (Maynard Smith
and Price 1973). Finally, in 1975 E.O. Wilson published Sociobiology,
which was a colossal documentation of social behaviour among ani-
mals including humans (Wilson 1975), which set off the contentious
sociobiology debate about the place of evolutionary models in the
study of human behaviour.
1.4.4 Calling genes selfish

Clinton Richard Dawkins was born in 1941 in Nairobi, in what was
then The Colony and Protectorate of Kenya and part of the British
Empire (Dawkins 2013a, 2015a). He spent his early years in southern
Africa, with his family in Nyasaland (now Malawi) and as a boarder in
Rhodesia (now Zimbabwe). T he family returned to England when he
was eight. In 1959 he enrolled at the University of Oxford, where he
(with the exception of a brief stint as a faculty member at the
University of California, Berkeley) would spend his whole professional
career. After receiving his doctorate for a thesis on decision making in
chicken supervised by the Dutch ornithologist and future Nobel
Prize winner Niko Tinbergen (Dawkins 1966), he subsequently rose
through the ranks at the Department of Zoology, being appointed
lecturer in 1970 and reader in 1990. In 1995, he became the first
Simonyi Professor for the Public Understanding of Science, a position
he held until his retirement.
As the author of numerous best-selling books and presenter of

award-winning documentaries on the subject of evolution, creationism,
and atheism, Dawkins is a strong contender for the most famous
evolutionary biologist alive. In 1966, however, when Tinbergen was
leaving for a sabbatical and asked him to take over his lectures on
animal behaviour, he was young, inexperienced, and very nervous.
Having never lectured to large groups of undergraduates before, he
took the time to type out his notes in order help himself stay on track,
in particular when navigating the tricky waters of Hamilton’s recently
published theory of inclusive fitness (Dawkins 2013a, p. 196). Looking
at these notes today, the rhetoric that would characterize much of his
subsequent writing is quickly noticeable:
Genes are in a sense immortal. T hey pass through generations, reshuf-

fling themselves each time they pass from parent to offspring. The
body of an animal is but a temporary resting place for the genes; the
further survival of the genes depends on the survival of that body at
least until it reproduces and the genes pass into another body (. . .) the
genes build themselves a temporary house, mortal, but efficient for as
long as it needs to be (. . .) To use the terms ‘selfish’ and ‘altruistic’ then,
our basic expectation on the basis of the orthodox neo-Darwinian
theory of evolution is that Genes will be ’selfish.
(Retold in Dawkins 2013a, p. 264; Original emphasis).
This is where the idea of ‘selfish genes’ is born. Despite being pub-
lished in the same year as Dawkins was preparing his lectures, he
would not read Adaptation and Natural Selection until a few years later.
He immediately recognized the intellectual bond between their world
views. Many of the ideas in The Selfish Gene are present in Adaptation
and Natural Selection, but to Dawkins, the way Williams expressed ideas
was ‘too laconic, not full throated enough’ (Dawkins 2016, p. xxiii).
As will be become clear in the next few chapters, however, calling
genes selfish is in equal parts helping and harming in communicating
that point. The term ‘gene’s-eye view’, which I have used throughout
this book, would not, to the best of my knowledge, appear until in
1980 in a paper by David P. Barash on evolutionary approaches to
understanding human families (Barash 1980, p. 187). Barash coined

the term borrowing from the expression ‘God’s-eye view’ (D.P. Barash,
personal communication) in an attempt to apply Hamilton’s work on
kin selection to humans.
1.5 Summary
• The gene’s-eye view takes adaptation, the appearance of design in

living world, to be the central problem a theory of evolution needs
to explain. This tradition has been particularly strong in British
biology, much thanks to the strong standing of natural theology and
the writings of William Paley.
• A gene’s-eye view can in retrospect be said to be implicit in the
writings of Haldane and Wright, but it is clearly explicit in Fisher’s.
In particular, Fisher (1918) introduces a subtle but radical shift in
what should be considered the environment and is arguably the first
paper to make use of a gene’s- eye view. Fisher’s Fundamental
Theorem of Natural Selection also makes the most sense when
adopting a genic perspective.
• Group selection has a tumultuous history and the levels of selection
debate provided the impetus for George Williams and Richard
Dawkins to write Adaptation and Natural Selection and The Selfish
Gene respectively.
2
Defining and Refining
Selfish Genes
2.1 Introduction
A round the time of its publication, The Selfish Gene’s editor

Michael Rodgers was discussing the book’s prospects with his
colleague at Oxford University Press, Richard Charkin. The initial
print run was 5,000 copies, but Charkin thought it would struggle to
sell more than 2,000. Rodgers, the optimist, promised to pay Charkin
£1 for every 1,000 copies sold under 5,000, and Charkin was to buy
Rodgers a pint of beer for every 1,000 copies over 5,000. To date, the
book has gone through four editions, been translated into twenty-five
languages, and sold well over a million copies. As Charkin puts it, he
is ‘holding back payment in the interests of [Rodgers’s] health and
well-being’ (Rodgers 2013, p. 53). Similarly, half a century on, Adaptation
and Natural Selection remains in print: 1996 saw the publication of a
30th anniversary edition with an updated preface by George Williams,
and 2018 another paperback edition with a new foreword by Richard
Dawkins.
Both Adaptation and Natural Selection and The Selfish Gene were
widely reviewed.Williams was highly praised in the scientific literature
and the book received very favourable reviews. Richard Lewontin
called it ‘excellent’ in Science (Lewontin 1966) and Lawrence Slobodkin,
though he had quibbles with some of Williams’s conclusions, titled his
DOI: 10.1093/oso/9780198862260.003.0003
De f i n i ng a n d r e f i n i ng se lf ish ge n es 47
long review in The Quarterly Review of Biology ‘The light and the way
in evolution’ (Slobodkin 1966). The Selfish Gene amassed over 100
reviews, both in the popular press and scientific journals, most of
which were positive (Dawkins 2013a, p. 281). The New York Times, for
example, described it as ‘the sort of popular science-writing that
makes the reader feel like a genius’ (Anonymous 1977).
In contrast to Adaptation and Natural Selection, The Selfish Gene
also attracted some very strong and contrasting views.W.D. Hamilton
wrote an enthusiastic review for Science (Hamilton 1977a) saying
that the book ‘should be read, can be read, by almost everyone’.
Charles Langley, on the other hand, wrote a scathing review for
Bioscience, calling it ‘shallow and untrue to the science of evolution-
ary biology’ and ‘a nuisance to the knowledgeable reader and mis-
leading to the layman’ (Langley 1977). Along the same lines, Richard
Lewontin’s review for Nature (Lewontin 1977a) was entitled
‘Caricature of Darwinism’ and called Dawkins’s adaptationist thesis
‘Panglossian’ (2 years before the Spandrels of San Marco paper with
Stephen Jay Gould), and also singled out the journal the American
Naturalist as an especially egregious home of this habit. The tone of
Lewontin’s writing led Hamilton to pen a letter of protest to the
editor, where he called the review a ‘disgrace and compared it to
Bishop Wilberforce’s attack on Darwin and Huxley at the British
Association meeting in 1860 (Hamilton 1977b). Lewontin shot
back equally pugnaciously, arguing that Hamilton himself was
responsible for his ‘fair share of vulgar Darwinism’ (Lewontin 1977b).
Hamilton, Lewontin suggested, was no Darwin and Dawkins was
no Huxley.
It also says something about the character of the two books that
early on they attracted the attention not only of biologists, but also
that of philosophers. Up until this point, the philosophy of science
was very much centred around the philosophy of physics (see
Mayr 1969 for an early version of this complaint). Anyone going
through the defining texts of Karl Popper and Thomas Kuhn looking
for insights into the nature of biological theories would be left wanting
(although see Niemann 2014 for an account of Popper’s 1986 Medawar

Lecture on evolution). Today, the situation is very different. In an
introductory essay accompanying the 50th anniversary edition of
Kuhn’s The Structure of Scientific Revolutions, the leading philosopher of
science Ian Hacking describes biology as having replaced physics as
science’s ‘top dog’ (Hacking 2012, p. xv).
Both Adaptation and Natural Selection and The Selfish Gene were
instrumental in the emergence of philosophy of biology as a distinct
field of study. Elliott Sober, one of the scholars who defined the field,
has described how he came to the philosophy of biology after being
intrigued by the philosopher William Wimsatt’s review of Adaptation
and Natural Selection (Wimsatt 1970; Marshall 2016). Sober would later
go on to grapple with many of the same issues in his influential The
Nature of Selection (Sober 1984). Other field-defining books, such as
Elisabeth Lloyd’s The Structure and Confirmation of Evolutionary Theory
(Lloyd 1988), Robert Brandon’s Adaptation and Environment (Brandon
1990), and Daniel Dennett’s Darwin’s Dangerous Idea (Dennett 1995), all
dedicated large chunks to issues that had been raised by Williams and
Dawkins: causality, altruism and selfishness, and levels of selection.
Combined, these issues have spawned a rich and sprawling litera-
ture. Over the years, proponents and critics of the gene’s-eye view
have also developed a vocabulary that can bewilder. This chapter is
dedicated to clarifying and untangling these terms.
To start, because the gene’s-eye view envisions the history of life as
a struggle between competing selfish genes, I will outline how this
definition of a ‘gene’ differs from that used in molecular biology.
Whereas in molecular biology, a gene has often been thought of as
encoding a particular RNA or protein that then has a function,
Williams and Dawkins advanced a definition a gene is defined as any
part of a chromosome that is not broken up by recombination and is
therefore passed on intact across generations. This definition is
sometimes called the replicator concept, where replicators are entities
whose structure is passed on intact across generations. Replicators are
then complemented with vehicles, which are cohesive wholes that
interact with the environment (a role typically played by individual

organisms) and so cause replicators to be passed on. Thus, replicators
cover one specific aspect of selection, transmission of hereditary
information, whereas vehicles cover the other, ecological aspect.
Next, both Dawkins and Williams emphasized that the key property
of a gene is not its physical properties, but its informational content.
Defining genes in this non-material way was central to the develop-
ment of the concept of memes, and I will include a brief discussion of
this. Although the last few years have seen the term meme come to be
associated with the rise of social media, Dawkins coined it in the last
chapter of The Selfish Gene to serve as a unit of cultural transmission,
a cultural replicator parallel to that of genes in organic evolution.
I will show why despite the attempts to free replicators from the con-
straints imposed by the material basis of genes, those physical details
are in fact key to understanding why the gene’s-eye view has been so
successful in the study of organic evolution but has failed to have a
similar influence on the study of cultural evolution.
Finally, I will end the chapter by comparing how the concept of
replicators and vehicles holds up next to other attempts to develop
abstract formulations of evolution and natural selection, such as
Lewontin’s principles, and how the gene’s- eye view fits into the
contemporary major transitions research programme.
2.2 What is a selfish gene?
Under the gene’s-eye view, fundamental terms are often defined in

unusual ways. In a series of publications, David Haig has argued that
accounting for these unusual definitions is key to understanding and
getting the most out the concept (Haig 1997, 2006a, 2012, 2020). In
Chapter 1, I discussed how Fisher introduced a radically expanded
notion of the environment. Here, I will take a starting point in Haig’s
work to outline how another familiar term—the gene—took on a
special meaning. Haig’s telling of the memetic history of the gene
begins not with Gregor Mendel, as deserving as he is of his place in the

history of genetics, but with the Dane Wilhelm Johannsen. In 1910,
Johannsen had been invited to attend the meeting of the American
Society of Naturalists, which that year took place in Ithaca, New York.
Despite being unable to attend in person, he nevertheless submitted a
contribution to the society’s journal and the paper appeared the fol-
lowing year ( Johannsen 1911). His central motivation for writing the
paper was that he thought that the study of heredity was hampered by
an outdated terminology. In particular, he considered biometricians,
such as Karl Pearson, to be too focused on the observable correlation
between parents and offspring and to pay too little attention to the
mechanisms that might cause the correlation. He contrasted this ‘trans-
mission conception’ of heredity with his own ‘genotype conception’
and argued that shifting from the former to the latter was crucial in
order to turn the study of heredity into an ‘exact science’.
Building on the recent rediscovery of the work of Mendel,
Johannsen introduced the distinction between the observable traits,
which he called ‘phenotype’, and the heritable factors, which he
dubbed ‘genotype’. A gene, then, was: ‘nothing but a very applicable
little word, easily combined with others, and hence it may be useful
as an expression for the “unit-factors,” “elements” or “allelomorphs”
in the gametes, demonstrated by modern Mendelian researches’
( Johannsen 1911).
Since Johannsen, ‘gene’ has taken on a diversity of more precise
meanings (Falk 1986; Griffiths and Stotz 2013; Kampourakis 2017). In
his Nobel prize lecture delivered some 20 years after Johannsen had
coined the terms phenotype and genotype, Thomas Hunt Morgan,
winner of 1933 prize in Physiology or Medicine for his work on the
role of chromosomes in heredity, noted that: ‘There is no consensus of
opinion amongst geneticists as to what the genes are—whether they
are real or purely fictitious’ (Morgan 1935).
The long-standing lack of a common definition of what a gene is
has resulted in a number of situations of biologists talking past each
other. The risk of mutually frustrating conversations seems to be
particularly high when evolutionary and molecular biologists get

together. One prominent example of such an incident is the molecular
biologist Gunther Stent’s reaction to reading Dawkins’s definition of
a gene in The Selfish Gene. Dawkins, following Williams in Adaptation
and Natural Selection (Williams 1966, p. 24), defined a gene as: ‘any
portion of chromosomal material that potentially lasts for enough
generations to serve as a unit of natural selection’ (Dawkins 1976,
p. 28). To Stent, the great sin of the Williams–Dawkins’s gene concept
was its vagueness on the molecular details. In his review of The Selfish
Gene, he described the definition as ‘denaturing the meaningful and
well-established central concept of genetics into a fuzzy and
heuristically useless notion’ (Stent 1977).
In general, evolutionary biologists have typically showed little con-
cern for the molecular intricacies of genes. After all, population genet-
ics was developed long before the material basis of heredity was
determined to be a nucleic acid and with only a meagre understand-
ing of the relationship between genotype and phenotype. In so doing,
they used a gene concept much closer to Mendel’s original ‘factors’.
Here, a gene is simply something that is statistically associated with a
difference in phenotype. Alfred Sturtevant, a student of Thomas Hunt
Morgan and the first to construct a genetic map of a chromosome,
summarized it like this:
All that we mean when we speak of a gene for pink eyes is, a gene
which differentiates a pink eyed fly from a normal one—not a gene
which produces pink eyes per se, for the character pink eyes is
dependent on the action of many other genes. (Sturtevant 1915)
Sturtevant’s comment has been conceptualized in various ways.

Kitcher and Sterelny (1988), for example, referred to it as ‘genes as dif-
ference makers’. T he idea that a gene’s effect is revealed only by com-
paring it with an alternative also features in Fisher’s thinking. Recall
from Chapter 1 that Fisher calculated an allele’s effect by the partial
regression of a given phenotype on the number of alleles present (i.e.
0, 1, or 2 in a diploid). T
o capture this aspect of genes, Moss (2003)
introduced the gene concept Gene-P, the preformationist gene that

predicts phenotypes. Gene-P is in contrast with the developmental
Gene-D, which lies closer to the use of the term by molecular biolo-
gists, where the gene is a material thing defined by its molecular
sequence.Whereas Gene-P would be familiar to Mendel and Johannsen,
advances in the past half century would render a paper on Gene-D
incomprehensible to them. Lu and Bourrat (2018) use many similar
arguments in discussing the relevance of recent empirical discoveries
of epigenetic inheritance for the definition of genes but suggest the
terms evolutionary genes (following Griffiths and Neumann-
Held 1999) and molecular genes. The key take-home message is that
the gene’s-eye view wants to talk about genes in an abstract way and
happily accepts a bit of fuzziness regarding their physical basis.
The gene’s-eye view’s way of conceptualizing genes also has implica-
tions for how we think about phenotypes. Instead of belonging to
organisms, the traditional view of most biologists, phenotypes belong to
genes. ‘A gene’s effects are its phenotype’, as Dawkins (1982a, p. 4) put it.
A gene’s effect can therefore only be understood in comparison to some
alternative allele (Haig 2012; Lu and Bourrat 2018). If there is no alterna-
tive, there is, by definition, no phenotype. While this may initially seem
strange, it comes close to Johannsen’s original definition of a phenotype,
which explicitly considered distinguishable ‘types’ of organisms.
What happens to the notion of ‘genes as difference makers’ when
genes lack phenotypic effects? This is not just of philosophical interest
but becomes a real issue when genome-wide association studies reveal
little to no signal for most parts of the genome (Noble and
Hunter 2020). One response would be that a lack of effect implies
that such genes are not genes at all. Alternatively, one can take it to
mean that those genes will just not be subject to selection and that
their fate in the population will be determined by genetic drift.
Finally, adopting the gene’s-eye view’s gene concept brings us back
to Fisher’s expanded notion of the environment. Whereas molecular
biologists and ecologists are united in defining the environment as
that beyond the physical boundaries of the individual organism, from
an gene’s-eye view it includes that plus the other alleles at the same
locus, the rest of the genome, and the gene pool in the population: in
essence, ‘all parts of the world that is shared by the alternatives being
compared’ (Haig 2012; see also Sterelny and Kitchner 1988).
One benefit of transferring ownership of the phenotype from the
individual organism to the gene is that it allows one to consider
phenotypes beyond the body of the organism, such as extended
phenotypes (see Chapter 5).
2.2.1 How long is a selfish gene?

A question that arose early about the gene’s-eye view gene was how
long does a ‘portion of chromosomal material’ need to be to count as
a gene? Some, such as Peter Godfrey-Smith consider the lack of clear
lengths to be a fatal flaw of the gene’s- eye view gene concept
(Godfrey-Smith 2009, pp. 135–139). Again, Dawkins and Williams
appear rather relaxed about this point. Dawkins repeatedly empha-
sized that a gene can be of arbitrary length (Dawkins 1976, p. 35, 1982a,
p. 87) and Williams remarked that:
Various kinds of suppression of recombination may cause a major

chromosomal segment or even a whole chromosome to be transmitted
entire for many generations in certain lines of descent. In such cases
the segment or chromosome behaves in a way that approximates the
population genetics of a single gene. (Williams 1966, p. 24)
By this definition, then, the non-recombining parts of the Y and W

chromosomes, as well as the entire genomes of mitochondria and
asexually reproducing organisms can be considered one gene
(Haig 2012). A sexual genome, however, is not a gene according to the
gene’s-eye view, for recombination and crossing-over during meiosis
breaks it up into multiple fragments.
The answer to the question of the length of a selfish gene largely
hinges on the extent of linkage disequilibrium. In a field notorious
for its convoluted vocabulary, linkage disequilibrium is one of the
worst offenders. In short, it simply means that the frequency of

association between alleles at different loci is different from random.
Population geneticists like Montgomery Slatkin argued that the
presence of widespread linkage disequilibrium meant that it made
little sense to talk about genes in this way, that is as individual units
during sexual reproduction (Slatkin 1972).
The gene of the gene’s-eye view has also been challenged from the
opposite direction. If there is extensive recombination, no chromo
somal portion will be transmitted intact for long enough to act as a
unit of selection. At the limit, this would mean that there are exactly
four genes, the four constituent bases of nucleic acids: adenine, thy-
mine, guanine, and cytosine (Griffiths and Sterelny 1999, p. 80).
Dawkins refers to this objection as the ‘selfish nucleotide theory’
(Dawkins 1982a, pp. 91–92). His counterargument centres on empha-
sizing genes as ‘difference makers’. Because nucleotides cannot be said
to have a phenotype, in the way a longer DNA segment can, Dawkins
argues it still makes sense to talk about genes:
The single nucleotide (…) cannot be said to have a phenotypic effect

except in the context of the other nucleotides that surround it in its
cistron [the stretch of DNA that encodes a single polypeptide]. It
is meaningless to speak of the phenotypic effect of adenine. But it is
entirely sensible to speak of the phenotypic effect of substituting aden
ine for cytosine at a named locus within a named cistron. (…) Unlike
a nucleotide, a cistron is large enough to have a consistent phenotypic
effect, relatively, though not completely, independently of where it lies
on the chromosome. (Dawkins 1982a, pp. 91–92)
Another way to respond to the ‘selfish nucleotide’ charge is to con-

cede and embrace it. In Darwinian Reductionism: Or, How to Stop
Worrying and Love Molecular Biology, Alex Rosenberg attacks what he
regards as an ‘untenable dualism’ characterizing much contemporary
philosophy of biology (Rosenberg 2006). To Rosenberg, the dualism
in question arises because most philosophers of biology, and evolu-
tionary biologist for that matter, are physicalists. T
hat is, they believe
everything in the universe—matter and mind—is made up of physical
things. At the same time, however, they are often anti-reductionist in

the sense that they seek explanations at the level of biological phe-
nomena—genes, organisms, populations—rather than at the level of
chemistry and physics. Indeed, the inability to reduce biology to spe-
cial cases of physical laws is often presented as key to the autonomy of
biology as its own scientific disciple (e.g. Mayr 2004, pp. 26–28). Such
a dualism, Rosenberg argues, opens up the door to ideas like intelli-
gent design and vitalism (the idea that living organism are made up of
some non-physical matter making them fundamentally different from
non-living things).
To get around this, Rosenberg presents a spirited defence of reduc-
tionism. Of particular relevance here is his argument that natural selec-
tion should be considered a physical law that can operate at one or more
lower levels of aggregation. At the most basic level, selection will act on
aggregates of atoms and macromolecules and will favour those aggre-
gates that are the most stable and fastest at replicating. In principle, then,
the same process will apply all the way up to cells, individuals, and groups.
Rosenberg’s reasoning shows that the ‘selfish nucleotide’ is not necessar-
ily as absurd as it might appear at first glance, but his argument also part
of a larger, and for scientists slightly intimidating, discussion about reduc-
tionism in science in general and biology in particular. See, for example,
Nicholson and Dupré (2018) for a very different perspective.
2.2.2 Is a selfish gene a token or a type?

The tension between treating genes as faithfully transmitted difference
makers, agnostic about their material basis, or as physical object like a
stretch of DNA with discrete boundaries, cuts across many debates
about the gene’s-eye view. One way to make sense of this disagreement is
to use the philosophical distinction between type and token (Haig
2012, 2020; but see Mitchell 2003, pp. 63–74). To appreciate the differ-
ence between types and tokens, consider the two ways one can answer
the question ‘how many mitochondrial genomes does a human somatic
cell contain?’ The first answer would be 1, as the mitochondrial
genome is strictly maternally inherited and therefore all mitochon-

drial genomes in the human body are genetically identical, bar any de
novo mutations. T he genome type thus occurs exactly once. T he sec-
ond approach to answering the question would be to count the num-
ber of mitochondria in the cell in question. T he number of times the
genome token appears will depend on the exact cell type, ranging
from 0 in a red blood cell to around 2,000 in a liver cell.
Whether the gene’s-eye view is best formalized using the type or
token approach has been subject to debate. Gardner and Welch (2011)
opted for the latter approach and used the mathematics of optimiza-
tion theory to develop a model of the gene as an inclusive fitness-
maximizing agent. Here, the gene is a physical object, a stretch of
DNA. The central conclusion of this analysis is that the gene does not
necessarily behave selfishly; it may also behave altruistically or spite-
fully towards other genes. They therefore argue that the only way to
retain the ‘selfish’ in ‘selfish genes’ is to define selfishness in the trivial
sense of being evolutionary successful (see also Noble 2011;
Gintis 2014, 2016, pp. 185–224).
Haig has conceived of genes as types in his ‘strategic gene’ framework
(Haig 2012, 2020). This approach takes seriously Dawkins’s comment
in The Selfish Gene: ‘What is the selfish gene? It is not just one single
physical bit of DNA (…) it is all replicas of a particular bit of DNA
distributed throughout the world’ (Dawkins 1976, p. 95). One conse-
quence of the type approach is that it does not make sense to think of
a gene as being physically located in an individual body. Instead, to
Haig, the strategic gene is the collective of all tokens whose chance of
transmission is affected by a given token. T he actor token and the
recipient token(s) may be physically in the same organism, but the
approach works equally well if they are not (see discussion of green-
beard genes in Chapter 5).
Whether one prefers types or tokens is partly a matter of taste. The
token approach has the benefit of a rich tradition of mathematical
modelling of social evolution at the organismal level (Gardner 2014a).
Thinking in terms of gene tokens having different inclusive fitness
agendas may be particularly useful when studying genomic conflicts

(see Gardner and Úbeda 2017). The type framework, in contrast, is
closer to Dawkins’s original argument. T he notion that genes’ ultim
ate goal is to increase their frequency in the population also only
really makes sense if the genes are types (Okasha 2019), as only gene
types (that is, alleles) can have a frequency. Again, this emphasizes the
point made in Chapter 1, that a more accurate name for Williams and
Dawkins’s argument could be said to be the allele’s-eye view.
In general, both Gardner’s and Haig’s approaches are in line with
the general agential approach to evolutionary theory favoured by
Dawkins (Okasha 2018). I will return to the agency concept, and its
contentious role in the history of biology, in Chapter 3. With this dis-
cussion of genes in place, I now turn to the major conceptual advance
enabled by taking the gene’s-eye view: the distinction between repli-
cators and vehicles.
2.3 Replicators and vehicles
Like [the pretentious social climber in Molière’s 1670 play The

Middleclass Aristocrat] Monsieur Jourdain, who was astonished to
discover that he had been speaking prose all his life, Dawkins
may well be surprised to discover that he had committed an act
of metaphysics. (Hull 1981)
To the philosopher David Hull, Dawkins’s act of metaphysics was

the introduction of the replicator and the associated argument that
evolution by natural selections involves two central entities: replica-
tors and vehicles. Hull was the first to clearly state that the evolu-
tionary process could be conceptualized in this way (though he used
the term interactor, rather than vehicle; Hull 1980, 1981). Williams
had earlier distinguished between ‘genic selection and organic adap-
tation’ (Williams 1966, p. 124) and Hull’s insight is also implicit in a
much-quoted passage of The Selfish Gene about how genes control
bodies:
What was to be the fate of the ancient replicators? They did not die
out, for they are past masters of the survival arts. But do not look for
them floating loose in the sea; they gave up that cavalier freedom long
ago. Now they swarm in huge colonies, safe inside gigantic lumbering
robots, sealed off from the outside world, communicating with it by
tortuous indirect routes, manipulating it by remote control. T hey are
in you and in me; they created us, body and mind; and their preserva-
tion is the ultimate rationale for our existence. T
hey have come a long
way, those replicators. Now they go by the name of genes, and we are
their survival machines. (Dawkins 1976, p. 25).
This paragraph is notoriously purple, even after Michael Rodgers

toned down its first draft (Dawkins 2013a, p. 277). Personally, I have
always preferred the limerick version, first introduced by Dawkins at
a conference banquet and retold in The Ancestor’s Tale:
An itinerant selfish gene
said ‘bodies a-plenty I’ve seen.
You think you’re so clever,
But I’ll live forever.
You’re just a survival machine. (Dawkins 2004a, p. 61)
The central message in both passages is that replicators and vehicles play
separate roles in the evolutionary process. Replicators are any entities
whose structure and information are copied and faithfully transmitted
from parent to offspring, forming lineages across generations. A suc-
cessful replicator has three properties: longevity, fecundity, and copy-
fidelity (Dawkins 1978). In organic evolution, the role of replicator is
usually played by genes.
Vehicles, on the other hand, what Dawkins referred to above as survival
machines, are the entities in which genes are bundled together and that
interact directly with the external environment. T his role is typically filled
by individual organisms but may also be carried out by cells and, more
rarely, by groups. Under this formulation, then, natural selection is a process
in which some vehicles are more successful than others, leading to the
survival and proliferation of their replicators. T
o Hull and Dawkins, repli-
cator survival and vehicle/interactor selection are two sides of the same coin.
Not everyone has seen merit in the replicator–vehicle distinction.

Michael Ghiselin called it a ‘misleading metaphor in support of a
dubious metaphysical thesis’ (Ghiselin 1997, p. 147) and Conor
Cunningham dismissed it as ‘quasi-Cartesianism’ (Cunningham 2010,
p. 65; see also Goodwin 1994, pp. 29–34 for a similarly flavoured
complaint). In an early critique of the gene’s-eye, Stephen Jay Gould
stated that selection cannot ‘see’ individual genes, only individual
organisms (Gould 1977; see also Mayr 1963, p. 184 for a related argu-
ment against population genetics). That is, selection does not ‘care’
why an individual is successful, just that it is. To use Robert Brandon’s
terminology, the phenotype ‘screens off ’ the underlying genotype,
making only the former visible to selection (Brandon 1990,
pp. 83–85).
Thinking in terms of replicators and vehicles shows why this cri-
tique is mistaken for at least two reasons. First, selection can clearly see
individual genes in the case of selfish genetic elements and other
forms of genomic conflict (see Chapter 5). Second, Dawkins repeatedly
emphasized that replicators need vehicles to be transmitted:‘[replicators
do not] literally face the cutting edge of natural selection. It is their
phenotypic effects that are the proximal subjects of selection’
(Dawkins 1982b). It is fair to say, however, that Dawkins certainly
favoured replicators, and his disagreement with Gould was partly a
consequence of Gould’s interest in vehicles over replicators
(Istvan 2013).When reading The Selfish Gene one can also easily come
away with the impression that only replicators matter. T hough The
Extended Phenotype is more balanced, the stated purpose of that book
is to undermine the idea of organisms as a useful concept in evolu-
tionary biology. As Dawkins would later note that he created the
vehicle concept ‘not to praise it, but to bury it’ (Dawkins 1994b). His
preference for replicators is also reflected in the passivity inherent in
the term vehicle. A vehicle, Dawkins argued, ‘can be regarded as a
machine programmed to preserve and propagate the replicators that
ride inside it’, and its passivity is ‘paradoxically why vehicle is a better
name than Hull’s “interactor” (1981). Interactor comes too close to
the (messy) truth and therefore does not merit a helpfully decisive
burial’ (Dawkins 1994b). In contrast, Hull preferred interactor as it
was more balanced in its relation to replicators (Hull 1980, 1981).
Rather than being mere ‘survival machines’ and ‘lumbering robots’ for
replicators, interactors play an active role in their environment.Vehicles
and interactors, though related, are thus not equivalent.
2.3.1 Lloyd’s four questions and the immortality

of replicators
Recall from Chapter 1 that proponents of the gene’s-eye view identify
the appearance of design in the living world as the central problem of
evolutionary biology. T o Dawkins, the way to address this problem is
to ask ‘when we say that an adaptation is “for the good of ” something,
what is that something?’ (Dawkins 1982b). T hat is cui bono? Or what
is the beneficiary of natural selection? This is what Elisabeth Lloyd
referred to as a ‘specific ontological issue of benefit’ or the beneficiary
question (Lloyd 2017). As a philosopher, Lloyd did an enormous job
in clearing up and sharpening the debate about units and levels of
selection, a debate that was long plagued by strong disagreements and
participants talking past each other (Lloyd 1988, 1989, 1992, 2017).
Lloyd’s crucial contribution was to distinguish the question of
benefit from three other questions that can be asked about the units
and levels of selection. In any given situation, Lloyd suggests that four
different questions highlight different aspects of the selective process:
1. What is the replicator?

2. What is the interactor?
3. Where is adaptation manifested?
4. What is the beneficiary of selection?
The first two questions correspond to the replicator and vehicle/

interactor distinction discussed above. Another way of asking the third
one would be: ‘When a population evolves by natural selection, what,
if anything, is the entity that does the adapting?’ (Sober 1984, p. 204).

This seems straightforward enough. For example, one may argue that
selection is really happening at the replicator level, but that it results
in adaptation at the individual or even group level. Alternatively, one
may require that adaptation at a given level is the product of selection
at that level (Sober and Wilson 2011).
The gene’s-eye view is based on the conviction that the beneficiary
question is the most important one. With this in mind, it is easier to
see why Williams and Dawkins were happy to accept such fuzziness
around their gene definition. T he gene’s-eye is primarily interested
the evolutionary origin of complex adaptations and trades in hard-
won molecular details of the structure of genes, for the ability to work
out the logic of natural selection. This trade-off pays off when natural
selection results in phenomena that makes little sense from the
perspective of individual organisms, such as worker sterility in eusocial
insects or genomic conflicts. When those molecular details matters,
such in many questions of developmental biology, the price of the
trade-off may be too high.
The centrality that they placed on the beneficiary question also
help make sense of why Dawkins and Williams put so much emphasis
on the unique properties of replicators. Chief among these properties
is that replicators are potentially immortal, as opposed to the transient
nature of vehicles. When Dawkins was looking for a publisher for
The Selfish Gene, he met with the influential editor Tom Maschler,
then at Jonathan Cape. Maschler liked the manuscript but not the
title and suggested The Immortal Gene as an alternative. This
change would capture much of the same message of the book but
avoid the word ‘selfish’, which Maschler considered a ‘down word’.
Dawkins would later think Mashler might have been right
(Dawkins 2006a, p. vii).
Replicators are the beneficiaries of natural selection because their
immortality means that are the entities that survive the evolutionary
process. Both Williams (1966, pp. 23–24) and Dawkins (1976, p. 34)
argued that while individual organisms measure their life span in
decades, replicators do so in thousands and millions of years. You

cannot have evolution within a single generation and only replicators
survive across generations. T he replicators that can be said to form
lineages across generations are those in sex cells, what Dawkins called
‘active germ-line replicators’ (Dawkins 1982a, p. 83). Any mutations in
somatic cells are considered dead-end replicators. Active germ-line
replicators are repeatedly subject to natural selection, generation
after generation. Organisms, however, are not. Whereas a mutation in
a successful replicator is transmitted, a change in an organism’s
phenotype⁠—a plant having one of its leaves chewed off by a caterpil-
lar, for example⁠—is not. As a consequence, only replicators have the
evolutionary persistence to be responsible for the cumulative selec-
tion required for evolution to result in adaptations.
The argument that only replicators, not organisms, form lineages
can be traced back to August Weismann’s idea of the ‘continuity of
the germ-plasm’ (Haig 2007). It was Weismann who introduced the
distinction between immortal germ line cells that produce sperm
and eggs and mortal somatic cells that die with the organism
(Weismann 1892). Weismann’s distinction was crucial to the rejection
of the Lamarckian idea of the inheritance of acquired characteristics,
as only changes to germ cells will be transmitted to the next generation.
In retrospect, his separation between the mortal body and the immor-
tal germ-line can be also seen as an early version of the replicator–
vehicle distinction. In this vein, Dawkins clearly acknowledges his
intellectual debt to Weismann early in The Selfish Gene (Dawkins 1976,
p. 11) and have later called him the ‘father of the selfish gene concept’
(Dawkins 1994a).
Today, the emphasis on active germ-line replicators appears overly
restrictive. T
here is increasing evidence that parents faithfully pass on
more than their genes (Bonduriansky and Day 2018). Moreover, while
only in its infancy around the publication of The Selfish Gene, the idea
that cancer is best thought of as an evolutionary phenomenon is
now clearly recognized (Stearns and Medzhitov 2015, chapter 6;
Aktipis 2020). T his is true even if it only involves somatic cells evolv-
ing within one organismal generation.
Genes are also not the only biological entity that have lifespans in
the millions of years, so do two others: species and traits. A crucial dif-
ference between species and replicators is that replicators affect what
vehicles survive and reproduce and therefore can be said to have agency
in the evolutionary process. Species cannot be said to play such a causal
role (Hampe and Morgan 1988; Lloyd 2017). Instead, they passively
benefit from the process of natural selection.
The trait challenge rejects the premise that cumulative selection
requires something to form lineages. By this argument, selection only
requires that something is persistently present across multiple generation,
a requirement satisfied by many phenotypic traits. T ake, for example, a
plant trait like the density of trichomes that prevents a leaf from being
eaten by caterpillars. T
he trait ‘trichomes’ may be present in a population,
though manifested on different individuals, for multiple generations, and
so satisfies the persistence requirement as outlined by Williams and
Dawkins. Indeed, studying traits across phylogenetic trees is at the heart of
the comparative method in evolutionary biology (Harvey and Pagel 1991).
Evolutionary longevity is thus not unique to replicators.
In response, proponents of the gene’s- eye view have therefore
emphasized another aspect that distinguishes genes from other
biological entities: information. Replicators are the only entities that
survive in the evolutionary process because they should be thought of
not as physical objects, but as units of information. As Dawkins put it
in The Blind Watchmaker:
It is raining DNA outside. On the bank of the Oxford canal at the
bottom of my garden is a large willow tree, and it is pumping downy
seeds into the air. (…) [spreading] DNA whose coded characters spell
out specific instructions for building willow trees that will shed a new
generation of downy seeds. (…) It is raining instructions out there; it’s
raining programs; it’s raining tree-growing, fluff-spreading, algorithms.
That is not a metaphor, it is the plain truth. It couldn’t be any plainer
if it were raining floppy discs. (Dawkins 1986a, p. 111)
This again shows why the type, rather than token, concept of genes
makes more sense for the gene’s-eye view. A gene token is no more
immortal than an individual organism.
There is an extensive literature on the concept of genes as

information (see e.g. Maynard Smith’s 2000 paper in Philosophy of
Science and comments from Godfrey-Smith 2000a, Sarkar 2000,
Sterelny 2000, and Winnie 2000). Williams argued that ‘evolutionary
biologists have failed to realize that they work with two more or less
incommensurable domains: that of information and that of matter’.
This message was a major theme of his 1992 book Natural Selection:
Domains, Levels, and Challenges. Towards the end of his career,Williams
would even say that he considered his work on the informational
aspects of the gene to be his major contribution to evolutionary
biology; if it was not for him, someone else would have come up with
the gene’s-eye view (Williams 1996b, p. 45). Similarly, a major reason
for why Dawkins preferred the term replicator over gene was because
it disentangled the concept from any material basis and allowed for
evolution by natural selection of other kinds of replicators (Dawkins
1982b; Dawkins 2006b, p. 228). In particular, Dawkins was interested
in the possibility of cultural replicators, what he dubbed memes.
2.4 Memes
Attempts to apply Darwin’s theory to cultural matters began soon

after the publication of the Origin of Species (reviewed in Lewens 2015
and Lewens 2018). In 1880, the American philosopher and pioneering
psychology educator Williams James wrote:
A remarkable parallel, which to my mind has never been noticed,
obtains between the facts of social evolution and the mental growth of
the race, on the one hand, and of zoological evolution, as expounded
by Mr Darwin, on the other. ( James 1880, p. 441; quoted in Lewens 2018)
James was writing in the context of a debate about ‘great men’ in his-
tory spurred by Herbert Spencer. Since then, many others tried to
develop more general accounts of cultural evolution. Early modern
attempts came from population geneticists like Cavalli-Sforza and
Feldman (1981), anthropologists like Boyd, and biologists like
Richerson (Boyd and Richerson 1985). T hough not the first or most

influential, memetics may well be the most famous attempt to use
insight from evolutionary theory to study cultural change (Aunger
2001; Lewens 2018).
Whereas the rise of social media has led to the term meme becoming
associated with both funny cats and right-wing frogs, its origin lies
elsewhere. The term was first defined in the last chapter of the first
edition of The Selfish Gene. (Though, unbeknownst to Dawkins, there
were some earlier uses of the term; see Laurent 1999.) Dawkins chose
the word meme because it resembled the word gene:
We need a name for the new replicator, a noun that conveys the idea
of a unit of cultural transmission, or a unit of imitation. ‘Mimeme’
comes from a suitable Greek root, but I want a monosyllable that
sounds a bit like ‘gene’. (Dawkins 1976, p. 192)
The central claim of memetics is that because organic evolution

requires something to play the role of replicator, so does a theory of
cultural evolution. Examples of memes suggested by Dawkins included
‘tunes, ideas, catch-phrases, clothes fashions, ways of making pots or of
building arches’ (Dawkins 1976, p. 206). The idea is that memes will
spread from mind to mind, with contagious ideas becoming more
common. The success of a given meme—say a new scientific or
religious idea about how the world works—will depend on how well
it fits the cultural environment in which it arises. In this way, the
success of a meme parallels that of a gene. While the gene’s-eye view
likes to think of individual genes, the only way to do this is by taking
into account what other genes are in the population. Memes can also
spread together in so- called memeplexes. Examples include
combinations of ideas, such as a political ideology.
Just as the gene’s-eye view opens our eyes to the idea that not all
genes may be working for the same purpose, thinking of culture in
terms of memes helps us see how harmful ideas may spread. Not all
memes will be beneficial to the vehicle that houses them. In the same
way that selfish genetic elements can spread despite the fitness cost to
the individual organisms, so can harmful memes. This is at the heart

of Dawkins’s description of religion as a virus of the mind
(Dawkins 1993b; Dawkins 2006b, pp. 218–219).
Memes as a theory of cultural evolution attracted both supporters
and critics. Daniel Dennett is a supporter and used it to develop a
theory of mind in Consciousness Explained (Dennett 1991). So is
physicist David Deutsch, who incorporated replicators (both genes
and memes) as one of the four strands of his ‘theory of everything’ in
The Fabric of Reality (Deutsch 1997). T he most ambitious attempt to
develop a comprehensive theory of memes remains Susan Blackmore’s
The Meme Machine (Blackmore 1999), a book with an almost
evangelical tone that came with a foreword by Dawkins. More
recently, the case for memetics was laid out by Stewart-Williams
(2018). A journal dedicated to the study of memes, The Journal of
Memetics—Evolutionary Models of Information Transmission, briefly
existed online from 1997 to 2005.
Critics of memetics have often been harsh. Ernst Mayr, for example,
dismissed it as little more than a renaming of the word ‘concept’
(Mayr 1997). T he philosopher and historian of ideas John Gray, who has
often incorporated insight from evolutionary theory in his work, went
further, comparing it to intelligent design and describing it as ‘a classic
example of the nonsense that is spawned when Darwinian thinking is
applied outside its proper sphere. (…) Talk of memes is just the latest in a
succession of ill-judged Darwinian metaphors’ (Gray 2008).
The idea of memes is an attempt to free the replicator concept from
the specific physical features of genes, yet those details show why the
replicator concept has been so influential in the study of organic but
not cultural evolution (Claidière and André 2012; Lewens 2015). T he
first problem concerns where the boundaries for what is considered a
single meme should be drawn (Daly 1982). This question arises when
discussing genes as well (see 2.2. What is a selfish gene?), but it can be
resolved by considering clear biological processes like recombination
and crossing over: a biological replicator is that which is stably i nherited
across generations. This kind of stability is much harder to achieve
with cultural entities (Sterelny 2006). Furthermore, the integrity of a

gene can be disrupted by mutation. In organic evolution, mutations
are essential for introducing new variation for selection to act upon.
A mutation rate that is too high, however, drowns selection with ran-
dom variation. Memes are therefore much likelier to fail to satisfy the
trio of properties of successful replicators: longevity, fecundity, and
copy-fidelity.
Next, memes, as opposed to genes, do not form lineages. Cultural
ideas reproduce in the sense that they are created again and again, and
thus there exists a meaningful way in which it is possible to talk about
a causal link between different creations, but not the sense that one is a
copy of another, like a gene (Wimsatt 1999; Sperber 2000). Whereas a
given gene token can in principle be traced back to the very point
where the mutation first arose, memes rarely or never work like this.
A final issue is how competition between memes is supposed to
work. Dawkins anticipated this problem: ‘memes seem to have noth-
ing equivalent to chromosomes and nothing equivalent to alleles’
(Dawkins 1976, p. 211). Competition among alleles at the same chromo
somal location is how the gene’s- eye envisions natural selection.
Mendelian inheritance, with occasional deviations for selfish genetic
elements, is thus crucial to the gene’s-eye view in the organic arena.
In culture, what plays that role? One response to this criticism is to
point out that in the early history of life, biological replicators were
not organized along chromosomes but may have floated free in pro-
tocells. Whereas meiosis is integral to how inheritance works in con-
temporary sexually reproducing organisms, it is in no way essential to
a theory of evolution, not even one based on the replicator concept.
Imposing this particular requirement on memetics is therefore unfair.
The contemporary study of cultural evolution is a thriving field
(Lewens 2015), though not without critics (Ingold 2007). Memetics
played an important role raising the field’s profile and it especially
highlighted that cultural practices may persist not because of the
benefit to the individual or the group performing them, but because
they have qualities that make them good at persisting regardless of
consequences.Yet, the above shortcomings mean that other theoretical

frameworks now dominate the field.
2.5 General formulations of evolution by

natural selection
In a 2015 essay, Dawkins argued that:
…if there is life elsewhere in the universe, it will be Darwinian life.

(…) This all comes about because at some point in history, about 4 billion
years ago, a replicating entity arose, not a gene as we would now see it,
but something functionally equivalent to a gene, which because it had
the power to replicate and the power to influence its own probability
of replicating, and replicated with slight errors, gave rise to the whole
of life. (…) So for me, the replicator, the gene, DNA, is absolutely key
to the whole process of Darwinian natural selection. So when you ask
the question, what about group selection, what about higher levels of
selection, what about different levels of selection, everything comes
down to gene selection. Gene selection is fundamentally what is really
going on. (Dawkins 2015b, pp. 1–2)
In so doing, he touched upon two issues that have played important

roles in disagreements over the gene’s- eye view. The first is the
assertion that evolution requires something to play the role of
replicator. Above and elsewhere Dawkins has argued that replicators
will be a feature of life, wherever it may be found in the universe
(Dawkins 2015a, p. 331). T he Dawkins–Hull formulation of replicators
and vehicles fit into a larger, more general, discussion about how best
to articulate the principles of evolution by natural selection in the
abstract. In contrast to Dawkins and Hull, many authors have
considered replicators to be a limited case and have tried to articulate
broader principles. T he second is whether gene selection a process or
a perspective. Above, Dawkins gives the impression that selection at
the gene level is a more factually true way to describe evolution than
selection at the organismal or group level. T his idea goes back all the
way to the earliest writings of Dawkins, but he has also on occasion
argued in favour of the weaker claim that the gene’s-eye view is but
one way of viewing the facts of evolution, no more true than an
organism-centred perspective.
Below, I tackle the issue of abstract formulations of evolution by
natural selection and I will return to the process versus perspective
issue in Chapter 3.
2.5.1 Lewontin’s Principles and limits of the

replicator–vehicle approach
Darwin originally formulated evolution by natural selection as
individual organisms engaging in a ‘struggle for life’:
Owing to this struggle for life, any variation, however slight and from
whatever cause proceeding, if it be in any degree profitable to an indi-
vidual of any species, in its infinitely complex relations to other organic
beings and to external nature, will tend to the preservation of that
individual, and will generally be inherited by its offspring. (…) I have
called this principle, by which each slight variation, if useful, is pre-
served, by the term Natural Selection. (Darwin 1859, p. 61).
It was quickly realized, however, that the abstract nature of the prin-
ciples of selection meant that it could operate at multiple levels and
even within organisms (see e.g. Huxley 1878). T he classic articulation
of this point was made by Lewontin (1970) and is now sometimes
referred to as Lewontin’s Principles (Brandon 2019). Lewontin stated
that evolution by natural selection requires three things:

1. Phenotypic variation. For a population to evolve, individuals
must vary in phenotype, such as morphology, physiology, or
behaviour.
2. Phenotypes must differ in fitness. Variation in phenotypic traits
must be associated with a difference in ability to survive and
reproduce.
3. Fitness is heritable. The fitness of parents must be causally correl
ated with that of their offspring.
John Maynard Smith developed an account very similar to Lewontin’s

and argued that the evolutionary process was built on a triptych of
‘multiplication, variation and heredity’ (Maynard Smith 1987). Both
Lewontin’s and Maynard Smith’s accounts function as conditional
statements. If a population satisfies these conditions, evolution by nat-
ural selection may occur. This approach has recently been expanded
to the concept of Darwinian Populations by Peter Godfrey-Smith
(Godfrey-Smith 2009; see also reviews by Pigliucci 2009; Dennett 2011;
Queller 2011; Sterelny 2011 and reply by Godfrey-Smith 2011 for an
overview of the debate to which this concept has led).
Godfrey-Smith classified his and Lewontin’s recipe approach as the
‘classic’ tradition to defining natural selection (Godfrey-Smith 2009,
p. 4). Together with life’s hierarchical organization (genes in genomes,
genomes in cells, cells in organisms, organisms in social groups), this
classic tradition is what gave rise to the levels-of-selection debate to
which the gene’s-eye view owes part of its existence. And it is in
contrast to this traditional view that the replicator–vehicle approach
of Dawkins and Hull should be understood. Their approach requires
two entities, replicators and vehicles, whereas the recipe version
requires only one. This difference in and of itself arguably means that
the recipe formulation is more general (Okasha 2008b). That being
staid, it does not take away from the fact that the replicator–vehicle
distinction has proved very useful for understanding a wide variety of
evolutionary questions. Instead, the replicator concept has other, more
serious, weaknesses.
One such weakness is that the recipe approach shows that genes are
‘optional’ to the evolutionary process. Whereas evolution requires
some sort of heritability, that is enough parent–offspring correlation
in traits to lead to cumulative evolutionary change, the mechanism
need not be the particular kind of inheritance found on this planet
(Godfrey-Smith 2000b). Okasha (2006, p. 15) referred to this as
‘Gould’s paradox’, following Gould’s argument that because Darwin
did not have a functioning theory of inheritance, but clearly
understood evolution, it does not make sense to treat replicators as
fundamental (Gould 2002, p. 613). Again, however, the fact that

evolution would work even under blending inheritance (though it
would require an extremely high mutation rate to avoid running out
of variation; Bulmer 2004) does not mean that the replicator–vehicle
concept is not helpful.
Take, for example, the concept of kin selection. Some authors have
argued the reason why Darwin himself did not develop a theory of
kin selection was that he was operating in a pre-Mendelian intellectual
world (e.g. Borello 2010). The main evidence for this claim is
Hamilton’s reliance on a gene’s-eye view when introducing the idea
(Hamilton 1963). Yet, as Gardner (2011) has convincingly shown, this
need not be the case. By deriving a kin selection model under the
assumption of blending inheritance, Gardner demonstrated that the
logic of kin selection does not rely on particulate inheritance. T he
key conclusion of his analysis is that the idea of kin selection could in
principle have been developed even in the absence of an understanding
of Mendelian genetics. Gardner’s conclusion comes with the caveat
that the analysis becomes more ‘tortuous’ under the assumption of
blending, rather than particulate, inheritance. Thus, just as for evolu-
tion in general, inheritance through genes is not required to under-
stand kin selection, but it certainly seems to make it easier to make
sense of many real life examples.
Another weakness is that the properties of replicators and vehicles
are themselves the product of selection. A requirement under the
Dawkins–Hull framework is that some entities have high enough
copy-fidelity to play the role of a faithfully transmitted replicator.
Some critics of the gene’s-eye view (e.g. Ball 2018) think that the
mutation rate in the earliest genes was too high for them to play the
role of a replicator. T
his objection is related to the issue identified
already by Manfred Eigen (independent of debates over replicators and
vehicles) that the mutation rate, measured in copying mistakes per base
pairs, becomes a lethal issue before a self-replicating molecule can
reach the length necessary to encode an enzyme that can correct such
mutations (Eigen 1971).While many solutions have been proposed, the
issue is hard to get around (Szathmáry 2006). Furthermore, the earliest

vehicles, probably some sort of simple unicellular organism or proto-
cell, were far from the cohesive entities implied by the vehicle concept
(Buss 1987; Michod 1999). T hus, the replicator–vehicle framework
suffers from the problem that its conceptual structure assumes some of
the empirical observations (such as the fidelity of replicator transmis-
sion or cohesiveness of individual organisms) that it is supposed to
explain (Griesemer 2000). As Denis Noble has emphasized, DNA can
typically not do much on its own but requires the infrastructure of the
cell to achieve anything (Noble 2018; see also Griesemer 2006). By this
argument, the separation of replicators as active and vehicles as passive
therefore gets things completely backwards.
The debate over units and levels of selection has since been trans-
formed from taking the hierarchy of life for granted to being con-
cerned with the evolutionary origins of this hierarchy. As Leo Buss
argued, ‘individuality is a derived character’ (Buss 1987, p. 14). T
he fact
that cells work together in multicellular organisms is not just a coinci-
dence, but the product of a series of evolutionary events. Explaining
the emergence of new levels in the hierarchy is the goal of the major
transitions research programme (Maynard Smith and Szathmáry 1995;
Michod 1999; Bourke 2011;West et al. 2015). How does the genes’-eye
view fare in this new world of major transitions? To that I turn next.
2.5.2 The major transitions and the levels

of selection debate
The major transitions research programme changed and re-energized
the levels of selection debate. Instead of taking the hierarchical
organization of life for granted, much effort is now devoted to explain
its evolutionary origins (see Okasha 2006 and Bourrat forthcoming).
The term ‘major transitions’ originally comes from John Maynard
Smith and Eörs Szathmáry, who published The Major Transitions in
Evolution in 1995 (and in 1999 a popular science version, or as Maynard
Smith put it: ‘a birdwatchers’ version’; Maynard Smith and Szathmáry
1999; Piel 2019). The definition of the term has changed slightly over
the years. Maynard Smith and Szathmáry (1995, pp. 3–4) defined them
as transitions ‘in the way in which genetic information is transmitted
between generations’ such that ‘entities that were capable of
independent replication before the transition can replicate only as
part of a larger whole after it’ (Maynard Smith and Szathmáry 1995,
pp. 3–4). This definition resulted in eight transitions:
1. Replicating molecules → Populations of molecules in compartments

2. Independent replicators → Chromosomes
3. RNA as gene and enzyme → DNA + protein (the genetic code)
4. Prokaryotes → Eukaryotes
5. Asexual clones → Sexual populations
6. Protists → Animals, plants, fungi (cell differentiation)
7. Solitary individuals → Colonies (non-reproductive castes)
8. Primate societies → Human societies (language)
To Maynard Smith and Szathmáry, what unified these major tran-

sitions was that they changed how the evolutionary process itself
operates by altering how heritable information is stored and trans-
mitted. Not all of their major transitions, however, involved the com-
ing together of previously independently replicating entities, now
known as evolutionary transitions in individuality and what most
contemporary researchers are concerned with (Clarke 2014;
Herron 2021; but see McShea and Simpson 2011). The evolution of
the genetic code is a good example of a change in the language, stor-
age, and transmission of information that is not an evolutionary tran-
sition in individuality.
Major transitions in individuality share two central features
(Maynard Smith and Szathmary 1995; Bourke 2011; West et al. 2015).
First, transitions in individuality involve the emergence of cooperation
among independent entities and lead to the formation of a new
higher-level individual entity. Second, crucial to the functioning of
this new level of individuality is the evolution of mechanisms to sup-

press conflict among lower-level entities.
Before The Major Transitions in Evolution was published, similar ideas
had been in the air for some time. In 1974, John Tyler Bonner grouped
the origin of the eukaryotic cell, multicellular organism, and social
groups as examples of complexity being the product of independent
units coming together to form new wholes (Bonner 1974). Next,
Buss’s The Evolution of Individuality was the first book-length treatment
of the modern hierarchical view and it focused on the evolution of
multicellularity (Buss 1987). Buss’s major contribution was to highlight
conflict suppression as the key to the origin and maintenance of a
new level of individuality. In the case of multicellularity, Buss paid
particular attention to the separation of the germline from somatic
cells as an adaptation to prevent selfish cells, like cancer cells, from
being passed onto the next generation. The emphasis on internal
conflict suppression turned the problem of hierarchy into a problem
of cooperation and brought it into the remit of social evolution.
At a conceptual level, Buss (1987) contrasted his hierarchical,
multilevel selection approach with the gene- centred approach of
Dawkins and Williams. T hough he clearly came down on the side of
the hierarchical approach, he stressed that the issue was primarily one
of taste: ‘to adopt a gene selection perspective is not wrong. It simply
does not help unravel the central dilemma of our science’ (Buss 1987,
p. 55). The case for a gene-centred approach to hierarchy was taken up
by Maynard Smith and Szathmáry. On this point they were unequivocal:
‘we are committed to the gene-centred approach outlined by Williams
(1966) and made still more explicit by Dawkins (1976)’ (Maynard
Smith and Szathmáry 1995, p. 8). The conflict between the two per-
spectives is, in some ways, exaggerated and several authors have argued
that the two are compatible and complementary (including
Queller 1997; Michod 1999; Okasha 2006; Bourke 2011). Not every-
one, however, took kindly to the gene’s-eye approach to hierarchy.
A review of Maynard Smith and Szathmáry (1999) in Nature by Gabby
Dover began:
One of the sadistic pleasures to be had from the defunct age of selfish-
genery was to witness the mental loops of its proponents as they tried
to extricate themselves from the illogical cul-de-sacs of their own
devising. In his writings, Richard Dawkins pseudo-‘paradox of the
organism’ was the climactic apotheosis of a belief in his own rhetorical
devices which forced him to suspend all scientific rationale and
modesty. (Dover 1999)
Dover went on to elaborate on this attack in his essay ‘Anti-Dawkins’

(Dover 2000). The ‘paradox of the organism’ that Dover refers to is
the paradox that despite all the opportunity for within organism-
conflict, the organism is ‘not torn apart by the conflicting interests of
the multitude of self-interested units that it contains’ (Dawkins 1990).
In fact, for many questions in evolutionary biology the consequences
of within-individual conflicts can typically be ignored and the indi-
vidual treated as a fitness maximizing agent. Dawkins was particularly
interested in parasites manipulating the behaviour of their hosts as an
example of extended phenotypes (see Chapter 5), but he clearly
appreciated the fact that the integrated cohesion of individual
organisms is not something that can be taken for granted, but is
something that demands an evolutionary explanation.
Overall, Dawkins’s own attitude to hierarchy appears somewhat
ambivalent. In the early 1980s, when he had just taken on the
editorship of the newly formed Oxford Surveys in Evolutionary Biology
together with Mark Ridley, he wrote to the palaeontologist Niles
Eldredge asking him to contribute a paper. At the time, Eldredge had
recently proposed the theory of punctuated equilibria together with
Stephen Jay Gould (Eldredge and Gould 1972) and was a major
proponent of hierarchical approaches to evolutionary theory (though
not those now associated with the major transitions). Eldredge replied
that he did indeed have an appropriate manuscript. But, he added,
‘you aren’t going to like this, this is all about hierarchy’. Dawkins
quickly wrote back saying ‘What makes you think I don’t like
hierarchy?’ Eldredge later said of the exchange: ‘[that was] a very
amusing and witty thing for him to write, because he’s such a gene
oriented, reductionist person. But he does talk about hierarchies, he

just handles them differently’ (Eldredge 1996, p. 91).
In The Selfish Gene, Dawkins clearly presents the gene’s-eye view as
an empirical alternative to (Wynne-Edwards style) group selection. In
The Extended Phenotype, this claim is toned down and, as Buss (1987,
p. 187) and Okasha (2006, p. 222) have pointed out, he unwittingly
engages in a bit of group selection theorizing himself in his discussion
of how the first replicators came together to form the first genomes
and cells. Dawkins clearly thought the origin of the first genome was
an interesting problem and once implored Maynard Smith to spend
more time developing game theory for replicators rather than
individuals (Dawkins 1978). Dawkins’s lack of clarity may well stem
from his always considering the interactor question as secondary to
the beneficiary question (cui bono).
On one point, though, Dawkins does not hesitate: genes are not the
lowest level in the hierarchy. Right after the appearance of The Selfish
Gene, Gould wrote:
challenges to Darwin’s focus on individuals have sparked some lively
debates among evolutionists. These challenges have come from above
and from below. From above, Scottish biologist V.C. Wynne-Edwards
raised orthodox hackles fifteen years ago by arguing that groups, not
individuals, are units of selection, at least for the evolution of social behav-
ior. From below, English biologist Richard Dawkins has recently raised
my hackles with his claim that genes themselves are units of selection,
and individuals merely their temporary receptacles. (Gould 1977)
In a similar vein, Elliott Sober and David Sloan Wilson argued: ‘A

proper understanding of the units of selection problem must take
account of an important symmetry: Just as organisms are parts of groups,
so genes are parts of organisms’ (Sober and Wilson 1994; original emphasis).
Dawkins would later admit that Gould’s comparison of him to
Wynne-Edwards tickled his ‘sense of mischief ’ (Dawkins 1982b), but
he also thought that Gould (and, by implication, Sober and Wilson)
was confused about the difference between replicators and vehicles:
‘[Gould] keeps going on about hierarchy as though the gene is the
bottom level in the hierarchy. T he gene has nothing to do with

the bottom level in the hierarchy. It’s out to one side’ (Dawkins 1996). T
o
Dawkins, there is no symmetry comparing his genes to Wynne-
Edwards’s groups. The individual versus group dispute was a matter of
empirical facts, falling under either Lloyd’s interactor or manifestor of
adaptation question. The gene, in contrast, was the answer to the
beneficiary question. Williams also maintained that comparing genes
and organisms leads you astray:
Until you’ve made the distinction between information and matter,

discussions of levels of selection will be muddled. Comparing a gene
with an individual, for instance, in discussions of levels of selection, is
inappropriate, if by ‘individual’ you mean a material object and by
‘gene’ you mean a package of information. (Williams 1996b, p. 44)
To Dawkins and Williams, genes really are special. Again, this conclu-
sion ties back to the type versus token distinction. T he gene token is
clearly at the bottom of the hierarchy and the only way to have the
gene be on the side is to adopt the type perspective where genes are
packages of information. Gould would later endorse Lloyd’s resolution
to the levels of selection question (Ketcham 2018), but the role of the
gene’s-eye-view’s replicator in major transitions remains contentious.
Some authors have argued that the major transitions are best approached
using multilevel selection analysis (Buss 1987; Michod 1999). This has
led the hierarchy to be compared to Russian matryoshka dolls with
layers of conflict and cooperation nested one within another (Wilson
and Wilson 2008). An alternative to multilevel selection models is
inclusive fitness analysis (Bourke 2011, 2014; West et al. 2015). What
all approaches have in common is a commitment to search for
common principles to answer the question that unifies all levels
(Ågren et al. 2019a): why does natural selection favour cooperation
rather than selfish behaviour that would undermine the integrity of
higher levels?
The problem with the Russian doll image is that in a matryoshka
doll there are dolls all the way down. Under the gene’s-eye view, this
is not how the biological hierarchy works (Bourke 2011, p. 59).

Whereas vehicles can be said to make up other vehicles, in the way a
multicellular organism is a group of cells, replicators (genes) play a
different role. As Dawkins put it above, the replicator is out to one side
(Dawkins 1996). Instead of Russian dolls, Bourke suggests that a more
apt description would be the children’s game ‘pass the parcel’. In this
game, a parcel is passed from child to child, each unwrapping one of
the many layers of wrapping paper. At the centre, however, is not
another piece of wrapping paper, but instead the gift, the parcel’s
actual purpose, or, to borrow Lloyd’s terminology, the beneficiary of
the whole unwrapping process.
In the biological hierarchy, genes are not just another level, but the
actual beneficiary of selection at all levels. Andrew Bourke has
explicitly argued in favour of a gene-centred inclusive fitness approach
to social evolution in general and the major transitions in particular
(Bourke 2011, 2014). In Chapter 4, I will examine the relationship
between the gene’s-eye view and inclusive fitness and argue that while
the two are intimately linked, there is also an under- appreciated
potential tensions between them.
2.6 Summary
• The gene of the gene’s-eye view is agnostic about molecular details

and is instead defined as a difference maker that is faithfully trans-
mitted across generations. Ignoring molecular details works best
when sorting out the logic of evolutionary scenarios with the goals
of answering the so-called beneficiary question.
• This gene concept can be generalized to replicators, which are
entities whose structure is passed on intact across generations. T o
fully capture the evolutionary process, replicators need to be com-
plemented by vehicles, which are cohesive wholes that interact with
the environment to determine reproductive success. In organic evo-
lution, vehicles are typically played by individual organisms, and
more rarely by cells and groups. Distinguishing between replicators

and vehicles turned out to be very helpful in moving the debate
about the gene’s-eye view forward.
• Memes were introduced to be a cultural replicator, equivalent to
genes in organic evolution. Despite being a hugely successful meme
in itself, memetics has had limited influence on the contemporary
study of cultural evolution.
• While the replicator–vehicle distinction may be less general than
the ‘classic’ recipe tradition of abstract formulations of natural selec-
tion, it has nevertheless been a very productive way to think about
evolution.
• The emergence of the major transitions research programme revi-
talized the level-of-selection debate. While the gene’s-eye view can
fit comfortably within the major transitions framework, the latter
has exposed further weaknesses in the replicator versus vehicle
distinction.
3
Difficulties of The Theory
3.1 Introduction
T he gene’s-eye view has been under intense scrutiny ever since its
conception. For one, the publication of The Selfish Gene only a
year after E.O. Wilson’s Sociobiology meant that it was immediately
caught up in the sociobiology debate. Public scrimmages included the
strange Isadore Nabi affair in the pages of Nature where a group of
biologists (believed to have been Richard Lewontin, Richard Levins,
Leigh van Valen, and Robert MacArthur) wrote under a pen name to
criticize sociobiology, including the gene’s-eye view (Nabi 1981a,
1981b; Lester 1981; Lewontin 1981; van Valen 1981; Wilson 1981; see
Segerstrale 2000, pp. 184–188).
Over in The New York Review of Books, Stephen Jay Gould and
Daniel Dennett had an ill- tempered exchange over the former’s
review of Helena Cronin’s The Ant and the Peacock in 1993. T he core
thesis of Cronin’s book was that the field of evolutionary biology had
collectively settled that the gene’s-eye view provided the key to two
long-standing problems: the evolution of altruism and sexual selection,
illustrated by the ant and the peacock respectively. Gould vehemently
rejected this conclusion. Titling his review ‘The confusion over
evolution’, he relegated gene selectionism to a ‘marginal position
among evolutionists’ (Gould 1992). Maynard Smith, who had written
the preface of Cronin’s book, was surprised by Gould’s tone and wrote
in to say so (Maynard Smith 1993). So too did Dennett, though he
DOI: 10.1093/oso/9780198862260.003.0004
Di f f icu lt i es of t h e t h eory 81
turned the rhetoric up a notch (Dennett 1993). In his reply, Gould

described Maynard Smith’s and Dennett’s letters as a ‘good-cop–bad-
cop grilling’ (Gould 1993). The section of the reply dedicated to
Maynard Smith began with a nod to ‘My dear colleague and good-
cop John Maynard Smith’ and referred to ‘the little community of
professional evolutionists (that John and I proudly call our own). . .’
The part of dedicated to Dennett, in contrast, opened with:
The less than collegial tone of Daniel Dennett’s commentary affirms the
worst suspicions bruited in some quarters about the pungently rarified
air of Cambridge, Massachusetts. (Thank God for Fenway Park and my
local Bowl-a-Drome, where these mental pirouettes can be temporarily
put aside and a semblance of populist normality attained.) Really,
Dan, however much you may find my views on adaptation distasteful,
why do you use this forum to air your personal grievances?
(Gould 1993).
Disagreements over the gene’s-eye view have often been heated. Not all
critiques, however, were aired in such public venues and with such bel-
licose rhetoric. Many of the criticisms were fair and reflected interesting
disagreements over how to think about evolution and natural selection.
Others were less so. In this chapter, I focus on some ‘difficulties of the
theory’, to borrow Darwin’s phrase, that have received much attention.
The first concerns an old sin of biology: anthropomorphizing. The
intentionality and personification involved in calling genes selfish has
grated critics inside and outside of biology since day one.While calling
genes selfish may seem innocent—‘because no sane person thinks
DNA molecules have conscious personalities’, as Dawkins (2016,
p. viii) put it—it does reflect a long-standing division within biology
about the role of teleology (explanations in terms of purpose and final
causes) and intentional language. Such language is common in evolu-
tionary biology but is viewed with deep scepticism by other biolo-
gists. I discuss this disagreement and argue that despite its weaknesses,
intentional language has an important role to play in biology.
The second concerns how the gene’s-eye view handles interactions
between genes. In The Selfish Gene, Dawkins develops an analogy
between genes in an organism and oarsmen in a rowing crew. He

argues that even if the coach is only basing their selection on how
successful each crew is, the coach is still selecting for the best individual
rowers. Critics argue that this is misleading. I use the rowing example
to discuss how the gene’s-eye view handles epistasis and heterozygous
advantage, and whether it commits the so-called averaging fallacy.
The third concerns the charge that the gene’s-eye view confuses
bookkeeping with causality. This is a long-standing criticism that
holds that just because the evolutionary outcome can be described as
a change in allele frequencies, it does not follow that causality is best
assigned to the level of genes. While biologists such as Stephen Jay
Gould popularized this criticism, much of the debate surrounding it
played out in the philosophical literature. I review the debate, showing
how it provides an informative account of the concept of pluralism in
evolutionary explanations.
The fourth concerns genetic determinism. This is the assertion that
the gene’s-eye view allows genes a too privileged role in accounts of
development. According to critics, genes play no special causal role
and biology needs a more inclusive notion of inheritance. The most
ambitious version of this claim has been put forward by developmen-
tal system theorists, in the light of which I evaluate where this leaves
the gene’s-eye view today.
The fifth concerns the concept of human nature and what evolution-
ary theory can tell us about human affairs. Evolutionary biology in
general has had a troubled relationship with both, and the notion of selfish
genes struck at the heart of it. T
his debate has recently calmed down, but
there are interesting parallels between the views of George Williams
and Richard Dawkins, and Darwin’s contemporary T.H. Huxley.
3.2 Anthropomorphizing
In 1979 the English philosopher Mary Midgley penned ‘Gene juggling’,

an infamous commentary on The Selfish Gene that began:‘Genes cannot
be selfish or unselfish, any more than atoms can be jealous, elephants

abstract or biscuits teleological’ (Midgley 1979). ‘Gene juggling’ was
not a book review, but a response to a paper on reciprocal altruism
that drew heavily on The Selfish Gene by another philosopher, John
Mackie (Mackie 1978). Still, Midgley’s tone was unusually harsh and,
perhaps unsurprisingly, Dawkins’s reply was cutting. In ‘In defence of
selfish genes’, he deploys his full stylistic repertoire (Dawkins 1981a).
It begins:
I have been taken aback by the inexplicable hostility of Mary Midgley’s
assault. Some colleagues have advised me that such transparent spite is
best ignored, but others warn that the venomous tone of her article
may conceal the errors in its content. Indeed, we are in danger of
assuming that nobody would dare to be so rude without taking the
elementary precaution of being right in what she said.
(Dawkins 1981a)
Dawkins goes on to describe how Midgley ‘raises the art of misunder-

standing to dizzy heights’ and lambasts her for her focus on humans,
which Dawkins admits being rather uninterested in (‘a particular, rather
aberrant species’). Midgley operated under the impression that Dawkins
actually thought that genes were selfish in the same way as humans are,
rather than in the more technical way used by evolutionary biologists.
An exasperated Dawkins asked:‘Did Midgley, perhaps, just overlook my
definition? One cannot, after all, be expected to read every single word
of a book whose author one wishes to insult’ (Dawkins 1981a).
Midgley’s paper represented an especially spurious misunderstand-
ing of the gene’s-eye view. In fairness, Midgley did later apologize for
the ‘impatient tone’ of article (Midgley 1983). She would go on to
develop a more nuanced take in her subsequent writings, such as
Evolution as Religion (Midgley 1985) and The Solitary Self: Darwin and
the Selfish Gene (Midgley 2010), though still viewing The Selfish Gene
as ‘a rotten essay in moral philosophy, propped up with bad scientific
examples’ (quoted in Brown 2016).
While this particular misunderstanding has never been particularly
widespread (but see, e.g., Stove 1992 and Stove 1995 for an effort to
keep the idea alive), the habit of ascribing goals, aims, and strategies to
individual genes tends to annoy certain kinds of biologists and
philosophers alike. For example, Rosenberg, who otherwise has been
very supportive of the gene’s-eye view, describes biologists using this
kind of language as ‘conspiracy theorists’ (Rosenberg 2011, pp. 13–14)
and Francis (2004, p. 8) and Godfrey-Smith (2009, p. 10) as suffering
from ‘Darwinian paranoia’. T he plant scientist David Hanke diag-
nosed the state of biology as follows:
Biology is sick. Fundamentally unscientific modes of thought are
increasingly accepted, and dominate the way the subject is explained
to the next generation. T he heart of the problem is that we persist in
making (literally) sense of a world that we now know to be senseless
by attributing subjective values to the objectives in it, values that have
no basis in reality. (Hanke 2004)
Hanke contrasts his own scientific training, which taught him ‘to
reason critically and objectively (. . .) and to regard the subjective as
untrustworthy and deceiving, potentially corrupting the truth’ with
the ‘tragedy’ that his undergraduate students have read nothing but
Dawkins before showing up in his classroom (Hanke 2004). The
students were all apparent victims of what Lucy Sullivan (1995) called
the ‘Oxford school of biological science fiction’. To Hanke and
Sullivan, the most egregious fault of anthropomorphizing, and inten-
tional language more broadly, is not just that it is ‘lazy and wrong’
(Hanke 2004) and whose ‘hegemony [is] quite out of proportion to its
intellectual finesse’ (Sullivan 1995), but that it leads us astray when
confronted with biological problems.
Disagreements about the role of anthropomorphizing, teleology,
and intentional language did not start with The Selfish Gene (Ruse 1989).
Instead, Hanke’s and Sullivan’s critique echoes a general argument
that such language is an embarrassment that makes biology look like
an immature science next to the likes of physics and chemistry. In
those subjects, they argue, theories are strictly physical and mechanical,
with all talk of purpose, goals, and intentions banished. Why should
biology be different?
This is in many ways a sensible question. Throughout the history of

biology, advances were often made by scientists who did not consider
biology to be anything special. For example, in the 17th century the
French philosopher René Descartes argued that living organisms were
nothing but machines that could be understood accordingly. This
quickly became the prevalent attitude, and many new discoveries
were made treating parts of organisms as parts of machines and then
asking how they all fit together (see Riskin 2016).
Another example of the non-uniqueness of biology comes from
Erwin Schrödinger What is Life? lectures delivered at Trinity College
Dublin in 1944. At that time the material basis of heredity was not yet
known. Part of the transformative value of the lectures laid in
presenting the problem of heredity as a physio-chemical problem like
any other. T his would end up having a profound effect on the audi-
ence and those who read the book subsequently published with the
same title. Two such young readers were Francis Crick and James
Watson who, together with Maurice Wilkins and Rosalind Franklin,
would later decipher the double helical structure of DNA. Both
credited Schrödinger for switching their research from physics and
ornithology, respectively, to molecular biology.
The discovery of the double helix in 1953 ushered in a golden age
of molecular biology. Associated with this was an influx of people and
methods from physics and chemistry. More recently, the flood of data
produced by whole genome sequencing and other technological
advances has attracted computer scientists, engineers, and statisticians
to the life sciences. This shift in biological research takes us back to
the question above, why should biology be different from other
sciences? Or, in other words, what, if anything, makes biology unique
as an autonomous scientific discipline?
The simplest answer is that biology is about organisms and organism
are special. Organisms are material things, made of the same fermions
and bosons as icebergs, and subject to the same physical laws as candle
flames. At the same time, they are unlike any other material thing.
Organisms appear to be endowed with a goal-directedness absent in
non-living things (Wilson 2005;Walsh 2015; Ruse 2018). It is therefore

in biology that purpose enters into scientific explanations. That
organisms make biology unique was also the answer Immanuel Kant
arrived at after much deliberation (Huneman 2007). T o Kant, it was
impossible to talk about biology without using purposeful language.
Kant did not believe that plants and animals actually possessed some
teleological or purposeful force. Instead, purpose is the most powerful
heuristic we have to talk about living things. Kant’s conclusion left
him rather disappointed and he glumly concluded that biology could
never be as proper a science as physics:
it is absurd to hope that another Newton will arise in the future who
will make comprehensible to us the production of a blade of grass
according to natural laws that no design has ordered. Such insight we
must absolutely deny to mankind. (Kant 1790, p. 228)
All of this changed with Darwin. In his theory of evolution by natural

selection, he provided an account of how a purely mechanistic process
can lead to the appearance of design in nature (Dennett 1995;
Haig 2020). Evolution by natural selection provides the bridge
between mechanism and purpose.
3.2.1 Reading Mother Nature’s mind and licensed

anthropomorphism
Although it can be appropriate to talk about purpose, to think in
terms of intentions, to anthropomorphize, this does not mean that all
ways of doing so are equally good. Like all heuristics, the goal of
anthropomorphizing is to make sense of old data and to generate new
empirically testable hypothesis about biological phenomena. Saying
that mosquitos bite because they dislike you, or that moths fly into
flames because they are depressed by the current state of political
affairs, do neither. That kind of naive anthropomorphizing is not
helpful.
Biologists have typically used two types of anthropomorphizing,
more accurately referred to as ‘agential thinking’ (coined by Godfrey
Smith 2009 and elaborated by Okasha 2018). The first conceptualizes

the process of natural selection itself as an agent trying to choose the
best individuals to survive and reproduce, analogous to a farmer
choosing the best stallion for breeding. T his tradition, which has been
referred to as ‘reading Mother Nature’s mind’ (Okasha 2018, p. 21),
goes back to Darwin himself who spoke of natural selection as
‘rejecting that which is bad’ and ‘preserving and adding up all that is
good’ (Darwin 1859, p. 83). He also made much of the parallels
between artificial and natural selection in The Origin of Species:
Under nature, the slightest difference of structure or constitution may

well turn the nicely-balanced scale in the struggle for life, and so be
preserved. How fleeting are the wishes and efforts of man! how short
his time! and consequently how poor will his products be, compared
with those accumulated by nature during whole geological periods.
Can we wonder, then, that nature’s productions should be far ‘truer’ in
character than man’s productions; that they should be infinitely better
adapted to the most complex conditions of life, and should plainly bear
the stamp of far higher workmanship? (Darwin 1859, pp. 83–84)
In retrospect, the use of the phrase ‘far higher workmanship’ is rather

Paleyan (Ruse 2019b, p. 39). Despite its distinguished origin, this kind
of thinking has some serious limitations. In particular, it may lead us
to believe that evolution has a goal and that natural selection acts with
foresight, both of which are clearly false.
In contrast, the second type of agential thinking has a lot going for
it. It conceives of biological entities, such as genes, cells, or organisms,
as agents pursuing goals. In contemporary evolutionary biology, this
approach is best represented by proponents of inclusive fitness who
argue that organisms should appear as if designed to maximize their
genetic representation in future generations and as captured by
modelling the maximization of inclusive fitness (Grafen 2007, 2014a;
Gardner 2009; West and Gardner 2013). Agential thinking at the
organismal level has proven to be especially popular in behavioural
ecology (see, e.g, Davies et al. 2012 for a textbook with it as its
conceptual backbone).
Assigning agency to genes may at first seem strange. Agency has

often been considered a defining distinction between the living
and the non-living (see, e.g., Soto and Sonnenschein 2020) and the
gene’s-eye view transfers agency from the paradigm living object—
organisms—to something non- living, genes. Moving beyond this
initial discomfort, agential thinking at the gene level finds its rationale
in helping biologists think about difficult problems. T he gene’s-eye
view helped make sense of old problems (Cronin 1991) and opened
our eyes to new ones (Chapter 5).
When assigning agency to genes, Dawkins repeatedly warned
readers to be cautious.With little success, it seems: ‘[Dawkins’s] caveats
slowed readers down about as effectively as “Slow—Work Zone”
signs on a deserted highway’, as Nesse (2006) put it. The importance
of caution was also at the heart of Dawkins’s reply to Lucy Sullivan’s
diatribe against anthropomorphizing in The Selfish Gene (Sullivant 1995;
Dawkins 1995a). Dawkins originally made the point as follows:
If we allow ourselves the license of talking about genes as if they had
conscious aims, always reassuring ourselves that we could translate our
sloppy language back into respectable terms if we wanted to, we can
ask the question, what is a single selfish gene trying to do?
(Dawkins 1976, p. 88)
What does ‘respectable terms’ mean? John Maynard Smith, when pressed
on this point in a Q&A-session following one of his talks, answered:
I am prepared to think as loosely as necessary to give me an idea when
I’m confronted with a new biological problem. If it helps me think to
say, ‘If I was a gene, I would do so-and-so’, then I think that is OK. But
when I’ve got an idea, I want to be able to write down the equations
and show that the idea works. (. . .) I’m all for loose thinking. We all
need ideas. (Maynard Smith 1998)
Dawkins and Maynard Smith emphasized the importance of both

having tools to support themselves as biologists thinking through
difficult problems and then translating their insights into a more
respectable form. The balance between anthropomorphic ‘loose
thinking’ and more formal reasoning, usually provided by mathematics,

is nicely captured by Grafen’s term ‘licensed anthropomorphism’
(Grafen 2003; though he coined it to refer to the idea that Fisher’s
Fundamental Theorem gives the license to think of organisms as
fitness maximizers). Licensed anthropomorphism comes close to my
own preferences in using a gene’s-eye view heuristic, coupled with a
simple population genetic model to show that the logic holds (such as
in Ågren et al. 2019b).
A good illustration of the value of licensed anthropomorphism
comes from the work of Manus Patten. In a recent paper, Patten
asked the simple question: should a mutation that arises on the
X-chromosome favour males or females? From a gene’s-eye view, it
can be predicted that because a X-linked gene spends two thirds of its
time in females, and only one third of its time in males (assuming an
XY sex chromosome system and a 1:1 sex ratio), that it generally
should favour females (Frank and Crespi 2011). Using a simple
population genetic model, however, Patten showed that you can get
the opposite result: mutations that favour males at the expense of
females can more readily spread in a population (Patten 2019). T his
comes about because in males each X-linked gene is present in only
one copy, and deleterious effects therefore cannot not be masked by
the other allele. Patten and Frank later synthesized their models to
show that we should expect a mosaic of both male and female biased
mutations on the X (Frank and Patten 2020; see also Hitchcock and
Gardner 2020). The exact distribution of the two will depend on
assumptions about dominance, dosage compensation, and the magni-
tude of sexually antagonistic selection.
3.3 Epistasis, heterozygote advantage,

and the averaging fallacy
One of the most famous analogies in The Selfish Gene is that of the
genome as a rowing boat and genes as oarsmen. The analogy starts
with the Boat Race that takes place annually between Putney and
Mortlake along the River Thames in London between the universities of
Oxford and Cambridge. Each team is made up of nine individuals, eight
rowers, and one cox who steers the boat. Winning requires oarsmen
who are not only individually accomplished but also capable of mesh-
ing as a team. How, then, should the coach select the team to balance
individual and team skills? Dawkins suggests the following strategy:
Every day [the coach] puts together three new trial crews, by random
shuffling of the candidates, for each position, and he makes the three
crews race against each other. After some weeks of this it will start to
emerge that the winning boat often tends to contain the same indi-
vidual men. These are marked up as good oarsmen. Other individuals
seem consistently to be found in slower crews, and these are eventually
rejected. But even an outstandingly good oarsman might sometimes
be a member of a slow crew, either because of the inferiority of the
other members, or because of bad luck—say a strong adverse wind. It
is only on average that the best men tend to be in the winning boat.
(Dawkins 1976, p. 40)
Moving back to genes. Competitors for each seat on the boat

correspond to alleles and rowing the boat to victory equals building
an organism with high fitness. In Chapter 1, I outlined how the
gene’s-eye view leads to an expanded definition of environment, one
that also includes non-additive genetic effects such as dominance and
epistasis. Selection will then favour genes that do well in the
environment provided by other genes. As Williams put it in Adaptation
and Natural Selection:
No matter how functionally dependent a gene may be, and no matter
how complicated its interactions with other genes and environmental
factors, it must always be true that a given gene substitution will have
an arithmetic mean effect on fitness in any population. (. . .) Adaptation
can thus be attributed to the effect of selection acting independently
at each locus. (Williams 1966, pp. 56–57).
When reading Williams’s and Dawkins’s writing above, the influence

of Fisher (1918), as well as Fisher (1941), really shine through. Even so,
in an interview with Ullica Segerstrale, Lewontin described the above

averaging strategy as ‘an epistemological error’ stemming from ‘a lack
of understanding of population genetics’ (quoted in Segerstrale 2000,
p. 277).
There are several points to disentangle here. One is about how
population size may affect the fate of alleles. T ake Dawkins’s comment
that appears after the oarsmen analogy is explained: ‘a gene which is
consistently on the losing side is not unlucky; it is a bad gene’
(Dawkins 1976, p. 41; original emphasis). T his addition is a little mis-
leading, as it would only hold true in a scenario where the population
size is infinite (or at least very, very large) and genetic drift is absent.
That is clearly unrealistic. Many features of genome evolution and
structure are likely due to genetic drift (Lynch 2007a).
A gene may also be unlucky because of population structure. For
example, if the trial crews in Dawkins’s example are not put together
at random, but instead certain oarsmen are more likely to be grouped
together than others, then the coach’s averaging strategy will not
work (Bar-Yam 1999). In general, this averaging strategy poses a
serious problem for the gene’s-eye view. In many situations, there
will be way more possible genotypic combinations than there are
atoms in the universe. While approximations will be of some help,
getting the true average effect of an allele on a phenotype will be
possible only in controlled lab experiments, not in most natural
populations.
An additional issue is the question of epistasis. Epistasis is another
one of those terms that can lead to frustration when molecular and
evolutionary geneticists interact, as it refers to different biological
phenomena in the two fields (Wade 1992). In molecular genetics,
epistasis happens when a mutation in one gene masks the expression
of another gene, as when a dominant allele masks the effect of a
recessive allele. In evolutionary genetics, however, it refers to the non-
additive component of genetic variance, which results from interactions
among different loci. In this particular debate, everyone is talking
about epistasis in the latter, statistical sense.
3.3.1 Ernst Mayr, Sewall Wright, and the

matter with epistasis
Echoing his critique of ‘beanbag genetics’, Mayr expressed the epista-
sis criticism of gene-centred approaches to evolution as follows:‘no
gene has a fixed selective value, the same gene may confer high fitness
on one genetic background and be virtually lethal on another’
(Mayr 1963, p. 296). To him, it made little sense to talk of the effect of
individual genes. He therefore repeatedly emphasized the concept of
‘unity of the genotype’ and the importance of ‘balanced complexes
that resist change’ (Mayr 1975; see Mayr 1997 for a summary of his
views on the issue).
As is often the case in the history of evolutionary genetics, the
disagreement over epistasis can be introduced as a disagreement

between Sewall Wright and R.A. Fisher. Wright and Fisher had
different views on many things, but the role of epistasis in adaptive
evolution was at the heart of one of their fiercer disagreements
(Provine 1986, Chapter 8). In his review of Fisher’s The Genetical Theory
of Natural Selection, Wright wrote that the two of them would be:
in exact agreement in all cases only if dominance and epistatic rela-
tionships were completely lacking. Actually, dominance is very common
and with respect to such a character as fitness, it may safely be assumed
that there are always important epistatic effects. Genes favorable in one
combination, are, for example, extremely likely to be unfavorable in
another. (Wright 1930).
Wright reiterated this view many times throughout his career, includ-
ing near the very end when, in his nineties, he used The Selfish Gene
to introduce a paper in Evolution (Wright 1980). Wright, as opposed
to Fisher and Haldane, was thus the only one of the three founders of
population genetics who lived long enough to comment directly
on the gene’s-eye view debate. While the paper primarily presents
Wright’s general views on the state of population genetics and his
contribution to the field, the paper was also intended to be a rejection
of the gene’s-eye view, which is how it has usually been read.Yet, the
paper itself touches only briefly on Williams, Dawkins, and Maynard

Smith, whom Wright lists as contemporary representatives of Fisher’s
views. Wright must therefore have wondered what to make of Peter
Medawar’s comment in the New York Review of Books that:
The most important single innovation in the modern synthesis was
however the new conception that a population that was deemed to
undergo evolution could best be thought of as a population of funda-
mental replicating units—of genes—rather than as a population of
individual animals or of cells. Sewall Wright (. . .) was a principal innovator
in this new way of thinking—a priority for which R.A. Fisher, an
important but lesser figure, never forgave him . . . (Medawar 1981)
Dawkins, however, admitted to ‘enthusiastically endorsing almost every

word’ of Mayr (1963) and of all of W
right’s (1980) arguments he disagreed
with ‘almost none’ (Dawkins 1982a, p. 238). Furthermore, Dawkins
argued that when the gene’s-eye view is properly understood, it leads to
an emphasis on genes’ ability to cooperate and indeed can offer not
only a version of Wright and Mayr’s views that they may find palatable,
but also a ‘truer and clearer expression’ of them (Dawkins 1982a, p. 239).
Dawkins returned to the rowing example later in The Selfish Gene
and discussed what would happen to the speed of the boat if the
oarsmen communicated with each other (Dawkins 1976, pp. 91–92).
Imagining a scenario where all oarsmen are monolingual, half English
speakers and half German speakers, Dawkins argued that the end-
result would be crews of only English speakers or only German
speakers. The absence of mixed crews, however, does not mean that
the coach selected on the crew as a unit. T he coach was still selecting
based on individual skill, but that central to that skill was the ability to
communicate with the other oarsmen in the same language. In
Unweaving the Rainbow, he went on to devote a full chapter, titled ‘The
selfish cooperator’, to the issue of genes cooperating (Dawkins 1998b,
pp. 210–234). He has also suggested that The Cooperative Gene would
have made for an equally good title as The Selfish Gene (a point with
which his editor Michael Rodgers strongly disagrees with to this day;
M. Rodgers personal communication).
Opinions differ on how successful Dawkins was with this explan

ation.Wade reviewed the mathematics of epistasis in light of the gene’s-
eye and suggested that it usually provides a too simplistic account of
the underlying genetic interactions (Wade 2002; see also Kamath 2009).
Similarly, Gould argued that the gene’s-eye view works ‘only if organ-
isms developed no emergent properties—that is, if genes built organisms
in an entirely additive fashion, with no non-linear interaction among
genes at all, [but] organisms are stuffed full of emergent properties’
(Gould 2002, p. 620). Discussing an earlier version of this argument
(laid out in Gould 1977), Dawkins maintained that Gould confused
genetics and embryology: ‘if this were really a good argument, it
would be an argument against the whole of Mendelian genetics, just
as much as against the idea of the gene as the unit of selection’
(Dawkins 1982a, p. 116). Dawkins noted that because genes are inherited
as discrete objects, any ‘blending’ (that is non-linear interactions
between genes) that may happen during development is irrelevant.
Dawkins’s and Gould’s disagreement is partly a reflection of their
different uses of the word ‘gene.’ As outlined in Chapter 2, the gene’s-
eye view’s abstract conception of a gene as a stably inherited difference
maker is quite different from the empirically informed definition pre-
ferred by Gould. T he weakness of Dawkins’s argument is that just
because genes are stably inherited it is not necessarily reasonable to
assume that that is the case for their ‘difference making’ qualities.
Dawkins’s Mendel-point holds under his preferred definition but
misses the point in light of alternative definitions.
3.3.2 Heterozygote advantage and the averaging fallacy

Sober and Lewontin’s paper ‘Artifact, cause and genic selection’ (Sober
and Lewontin 1982; see also Sober 1984, pp. 302–313) is one of the
most influential critiques of the gene’s-eye view. Even Maynard Smith
admitted to having been initially swayed by the paper, though in the
end he remained unconvinced (Maynard Smith 1987). Sober and
Lewontin’s argument was that while it is always possible to calculate
selection coefficients for individual genes, those are not actually real;
they are statistical artifacts.
To illustrate this point, they developed an example of heterozygote
advantage. Heterozygote advantage arises when the heterozygous
genotype (say, Aa) has a higher fitness than either of homozygous
genotype (AA or aa). The textbook example of heterozygote advan-
tage is the balancing selection acting on the gene involved in sickle-
cell anaemia and malaria resistance. Individuals homozygous for the
recessive allele develop sickle-cell, whereas heterozygotes are resistant
to malaria, resulting in both alleles being retained in populations with
high prevalence of malaria.
Sober and Lewontin used a simple one-locus two-allele model to
present their case. Consider the two alleles, A and a with no domi-
nance, that have frequencies p and q respectively (such that p + q = 1).
The population is assumed to be at Hardy–Weinberg equilibrium
prior to selection, and the fitnesses of AA, Aa, and aa are given by wAA,
wAa, and waa. The genotype frequencies after selection can be calcu-
lated by multiplying the initial genotype frequencies with their fitness
and then dividing by the population mean fitness, w (Table 3.1).
So far, fitness is a property of the diploid genotype, not of individual
alleles. Deriving the fitnesses of individual alleles (A and a), however,
is not particularly complicated. For example, if the fitness of A is
defined as WA, it can be calculated by averaging the fitness of A across
all genotypes in which it is found. Recall that A can occur with a
frequency of 1, 1/2, and 0 in AA, Aa, and aa respectively. Then, using
the frequencies and fitnesses defined above, and given that: the
Table 3.1. Sober and Lewontin’s heterozygote advantage example
Genotype AA Aa aa
2
Frequency before selection p 2pq q2
Fitness w AA w Aa w aa
Frequency after selection p 2w AA 2 pqw Aa q 2w aa
w w w
frequency of A after selection × w = wA × frequency of A before

selection, this gives:
w A = w AA p 2 + w Aa (1/ 2)2pq ) / ( p 2 + (1/ 2)2 pq ) = pw AA + qw Aa
Using the same method:
w a = w aa q + w Aa p.
wA and wa can then be used to predict changes in allele frequency.

Sober and Lewontin granted that this will work most of the time.
With heterozygote advantage, where wAa > wAA and wAa > waa, how-
ever, they argue that the approach fails. While individual selection
coefficients can readily be calculated in this case by averaging across
all genotypes, and both the individual gene model and the diploid
genotype model can predict future changes in gene frequencies, only
the latter accurately represents the causal forces at play.
To Sober and Lewontin, the problem is that A lacks what they call
a ‘uniform causal role’. In certain contexts it is favoured by selection
and it others it is not: ‘If we wish to talk about selection for a single
gene, then there must be such a thing as the causal upshot of possessing
that gene’ (Sober and Lewontin 1982). Sober and Lewontin’s argument
has later been referred to as the ‘averaging fallacy’ (Okasha 2004),
using a term coined by Sober and Wilson (1998, pp. 31–35). Sober and
Wilson originally used the term in the group selection debate to
criticize the suggestion that examples of group selection could be
recast as individual selection by calculating the fitness of an individual
by averaging its fitness across all the groups in which it is found.
(While the gene versus genotype situation may appear analogous to
the individual versus group one, there are crucial ways in which this
analogy fails, Okasha 2004; but see Winther et al. 2013 for an alternative
interpretation).
Several authors have defended calculating genic selection coeffi-
cients (including Rosenberg 1983; Maynard Smith 1987; Sterelny and
Kitcher 1988; Waters 1991; Weinberger 2011; see also Queller 2020).
The strongest defence is to concede that in the heterozygote advantage
example the allele’s effect is indeed context-dependent but to deny

that this is a problem. Many traits are context-dependent and as such
their fitness effects depend on their environment, which includes the
states of the other traits in the organisms in which they are found. As
explained above, under the gene’s-eye view the rest of the genome,
including the other allele in a diploid, is part of the environment.
According to the gene’s-eye view, then, the heterozygote case is no
different from any other environment-induced variance in the fitness
effect of an allele. While the gene’s-eye view may work best if the
effect of an allele is, or is close to being, independent of context
(Okasha 2006, p. 167), imposing a requirement of a ‘uniform causal
role’ is too stringent a condition.
3.4 The bookkeeping objection
In 2002, the year that he passed away, Stephen Jay Gould published
The Structure of Evolutionary Theory. A majestic book (it clocks in at
close to 1,500 pages) its vast scope touches on practically every aspects
of evolutionary biology, its history, and its philosophy. Joe Felsenstein
once remarked that ‘if you’re holding Gould’s book in your lap, stasis
is very real: you couldn’t possibly stand up under the weight of all that
verbiage’ (Felsenstein 2012). In a similar vein, Stephen Stearns recalls
bringing the book on a flight only to be asked by an air stewardess to
store the book in the overhead compartment so not to risk hurting
other passengers should he lose control of it during take-off and
landing (Stearns 2002).
As expected, a significant chunk of the book is dedicated to
explaining the perceived short-comings of the gene’s-eye view. In a
characteristically long-winded section, Gould writes that ‘the error
and the incoherence of gene selectionism (. . .) can be summarized in
a single statement (. . .) proponents of gene selectionism have confused
bookkeeping with causality’ (Gould 2002, p. 632; original emphasis). The
bookkeeping objection to the gene’s- eye view states that while
evolutionary change can be described as changes in allele frequencies

over time, one cannot necessarily conclude anything about the causes
of those changes. Just because the result of selection can be correctly
recorded at the gene level, it does not mean that it is the most
appropriate level of analysis. As Gould put it ‘selection is a causal
process, not a calculus of results’ (Gould 2002, p. 623).
Whereas the credit for coining the term ‘bookkeeping’ belongs to
Wimsatt (1980), it was advanced by several critics of the gene’s-eye
view (Sober and Lewontin 1982, 1983; Walsh 2004; Brosius 2005;
Brandon and Nijhout 2006). A version of this argument can also be
found already in Wright’s criticism of Fisher (Wright 1930). Sober and
Lewontin (1982) wrote that the genes’-eye view not only ‘fails to do
justice to standard textbook examples of Darwinian selection, it
‘distorts the causal process’, and simply ‘generates the wrong answers
to the question of what is happening’. T he wrong answer that Sober
and Lewontin have in mind is the gene’s-eye view’s desire to assign
causality to the level of genes for all selective events. To them, the level
at which causality belongs—gene, cell, individual, group—depends
the biological example under study, and the gene level should be
reserved for examples of genomic conflicts (see Chapter 5).
Gould probably did more than anyone to popularize the bookkeep-
ing objection (Gould 1994, 2002, pp. 632–637, Gould and Lloyd 1999).
Gould’s version of the argument start by conceding that genes are (in
some ways) special: the faithful transmission of genes makes them a
uniquely suitable entity to document the evolutionary history of a
population. On this, he fully agrees with proponents of the gene’s-eye
view. Furthermore, because genes are at the very bottom of the bio-
logical hierarchy (genes within cells, cells within organisms, organism
within groups, and so on) they possess an asymmetrical quality rela-
tive to other levels. That is, selection at higher levels also results in
selection at lower levels, which means that if frequencies of higher
levels shift, so do those of the lower levels. T
he reverse is not necessarily
true. Selection at the genic level, for example on selfish genetic elements
(see Chapter 5), may cause certain genes to increase in frequency
without having an effect on the species level (i.e. on the rate of speci
ation or extinction). Genes are thus the only level that can be said to
capture selection at all levels.
But, and to Gould this is the crucial but, this does not mean that
genes are the causal agents. Gould has argued Williams and Dawkins
both realized this, but that they refused to admit it (Gould 2002,
pp. 632–644). T ake, for example, Williams in Natural Selection:
For natural selection to occur and be a factor in evolution, replicators

must manifest themselves in interactors, the concrete realities that con-
front a biologist. The truth and usefulness of a biological theory must
be evaluated on the basis of its success in explaining and predicting
material phenomena. It is equally true that replicators (codices) are a
concept of great interest and usefulness and must be considered with
great care for any formal theory of evolution. (Williams 1992, p. 13)
And Dawkins in The Extended Phenotype:
Of course genes are not directly visible to selection. Obviously they are
selected by virtue of their phenotypic effects, and certainly they can
only be said to have phenotypic effects in concert with hundreds of
other genes. (Dawkins 1982a, p. 117; original emphasis).
Such reasoning Gould takes as evidence that even the most ardent
advocates for the gene’s-eye view actually agree with him: causality
belongs at the level of the interactors. Gould also cites the shift in
focus between The Selfish Gene and The Extended Phenotype as a case
in point. Early on, Dawkins clearly presents gene-level selection as a
(superior) alternative to group selection. For example, two years after
The Selfish Gene Dawkins wrote: ‘Evolutionary models, whether they
call themselves group-selectionists or individual-selectionists, are fun-
damentally gene-selectionists’ (Dawkins 1978). T
his is also the message
in Adaptation and Natural Selection (Williams 1966, pp. 123–124). In this
formulation, the gene’s-eye view is meant to be a uniquely true
description of how the world works.
The argument in The Extended Phenotype is different. In the first
chapter of the book, Dawkins introduces the Necker cube illusion.
Under this illusion, the human mind can see two images of a two-
dimensional line drawing of a cube, each equally ‘true’. The gene’s-
eye view and the traditional individual-centred view are thus different,
but equally valid, perspectives of evolution, just like the orientations
of the Necker cube. To Gould, this sounds like George Aiken, the
Republication senator from Vermont, who in the middle of the
American war in Vietnam, suggested that the US should just declare
victory and go home (Gould 2002, p. 638). Gould argues that Dawkins
admits defeat, the gene is not the one true unit of selection, but that
he still declares victory for the gene’s-eye view.
The disagreement over the bookkeeping objection reflects a
common confusion over whether gene selection is best regarded as a
process or a perspective. This is a confusion for which admittedly
Williams and Dawkins bear some responsibility. Dawkins argues that
the group versus individual selection debate is simply an empirical
disagreement over at what level selection is most effective in natural
populations (Dawkins 1982b). T he replicator versus vehicle distinc-
tion, on the other hand, is not. It is a question of perspective:
I am not saying that the selfish organism view is necessarily wrong, but
my argument, in its strong form, is that it is looking at the matter the
wrong way up. (. . .) I am pretty confident that to look at life in terms
of genetic replicators preserving themselves by means of their extended
phenotypes is at least as satisfactory as to look at it in terms of selfish
organisms maximizing their inclusive fitness. In many cases the two
ways of looking at life will, indeed, be equivalent.
(Dawkins 1982a, pp. 6–7)
So the replicator and vehicle perspectives may be equivalent. Does this

mean that Dawkins considers them to be equally useful? The answer is
clearly no. Remember that he said he coined the vehicle concept ‘not
to praise it, but to bury it’ (Dawkins 1994b). Indeed, a central goal of
The Extended Phenotype is to demonstrate the ‘theoretical dangers’ of
thinking in terms of individual fitness (Dawkins 1982a, p. 91).
Gould’s Aiken comparison is therefore rather uncharitable.Williams
and Dawkins has never denied that vehicles are often necessary for
evolution (though not always, see Dawkins 1994b). Again, Lloyd’s four

questions (Chapter 2) are helpful to make sense of the situation. To
Williams and Dawkins, the unit of selection question was never about
what entities play the role of interactors; instead they were interested
in Lloyd’s beneficiary of selection question.
3.4.1 Tempered realism and pluralistic gene selectionism

To many biologists, this is where the debate ended.While the field of
evolutionary biology has long wrestled with the concept of causality
(see, e.g., Otsuka 2016 and Uller and Laland 2019 for overviews),
many biologists, being primarily concerned with more practical
matters, seem to have been quite happy to sometimes think of selec-
tion in terms of genes and sometimes in terms of individuals. The
next phase of the debate over the bookkeeping objection therefore
took place primarily in the philosophical literature. There it fed into
a debate regarding whether a given selective event can always be
causally described in one, and only one, way or in several, equally
true, ways.
The idea of pluralism regarding selection is captured by Dawkins’s
Necker cube idea, that for any selection processes, there are multiple
equally adequate representations of the causal forces at work.‘We have
two images of natural selection’, as Kim Sterelny and Philip Kitcher,
put it, referencing the organism and gene-centred accounts (Sterelny
and Kitcher 1988). Together with Kenneth Waters’s PhD thesis Models
of Natural Selection from Darwin to Dawkins (Waters 1986), their paper
marked the start of the debate over what has become known as
pluralistic genic selectionism. Pluralism here contrasts with monism,
the idea that there is a uniquely correct way to causally describe a
selective event (Rosenberg 1993 makes this case). Genic pluralism
considers the search for the ‘true’ unit of selection to be a waste of
time, an ‘exercise in muddled metaphysics’ (Kitcher et al. 1990) and
they urge their colleagues to ‘turn their attention to more serious
projects than that of quibbling about the real unit of selection’.
Kenneth Waters has advocated the term ‘tempered realism’ to

describe this position (Waters 1991, 2005). The term comes about
because the pluralists are still committed to scientific realism, the
belief that science makes progress at describing true features of the
universe, but that these descriptions are not uniquely true. T hat is,
there may be multiple true causal models for a given biological
event, hence the need to ‘temper’ the commitment to realism. For
philosophers interested in causality this has been difficult to swallow.
Some of the strongest critics of genic pluralism have been Sober
(1990) and Lloyd (2005), and the latter’s exchange with Waters
(Waters 2005; Lloyd et al. 2005) reveals a debate that is very much still
alive (see Ketchum 2018 for a summary).
If different models make the same empirical prediction, can, as
Maynard Smith once put it, any good Popperian consider the matter
of choosing between models as anything other than pseudoscience?
(Maynard Smith 1987). There will be cases where one modelling
framework is genuinely better than another at capturing the causal
forces at work, but in others arguing over which one is correct would
be ‘as foolish as it would be to argue whether algebra or geometry is
the correct way to solve problems in science’ (Maynard Smith 1986,
p. 30). That being said, the equivalence of models is often achieved
only by comparing highly abstract statistical formalisms, rather than
models that explicitly casual. This, for example, is a problem with the
claim of equivalence between inclusive fitness and group selection
models (Clarke 2018; Birch 2019). T here is therefore a serious discus-
sion to be had about different modelling traditions in evolutionary
biology, not just why we prefer one framework over another, but also
what philosophical assumptions that lead us there (Otsuka 2019).
In a commentary on a paper that compared contextual and
collective approaches to modelling multilevel selection (Kerr and
Godfrey-Smith 2002), Maynard Smith demonstrates this admirably
(Maynard Smith 2002). Discussing how relatedness can be modelled
either using a gene- centred approach or through an individual-
centred approach using inclusive fitness, he notes that in general
having multiple mathematically equivalent models in mind at the

same time can be very helpful in making inferences about what is
going on in a given selective episode. He then remarks:
I confess that in this case I find the gene-centred approach both
mathematically simpler and causally more appropriate, but this may
merely reflect the fact that I prefer microscopic to holistic models:
Maxwell- Boltzmann to classical thermodynamics, and Dawkins to
Price’s equation. (Maynard Smith 2002).
Just because two abstract mathematical models yield the same predic-
tion does not mean they are causally equivalent. Regardless of your
views on the matter, Maynard Smith’s attitude is exactly the kind of
honest philosophical transparency that we need more of in evolution-
ary theory.
3.5 Genetic determinism
One of the most thoughtful critics of the gene’s-eye view over the
years was Patrick Bateson. Bateson, whose grandfather’s cousin
William Bateson gave science the word ‘genetics’, was an English
behavioural ecologist with a special interest in the developmental
biology of animal behaviour. Ever since he wrote a critical review of
The Selfish Gene (Bateson 1978), Bateson has been a reliable sparring
partner of Dawkins. When he contributed to the festschrift Richard
Dawkins: How a Scientist Changed the Way We Think (Grafen and
Ridley 2006), he was grouped under heading ‘Antiphonal voices’
(Bateson 2006a). The main message of Bateson’s critique was that too
much focus on genes over other factors contributing to the formation
of an animal obfuscates the true causes of development and so results
in a poorer account of evolution.
One of Bateson’s concerns was that the intentional language of the
gene’s-eye view may result in confusion regarding genetic determin-
ism, the idea that genes and only genes matter in determining pheno-
types. ‘Dawkinsspeak leads to Dawkinspractice’, as Gray (1992) once
put it. It’s not that gene-selectionists are committed to genetic deter-
minism, Bateson argued, but that sloppy terms like ‘gene for’, ‘blue-
print’, ‘genetic program’, and ‘hardwiring’ mean that one can be
forgiven for thinking that they are (Bateson 1981, 1999, 2001; Curley
et al. 2009; see also Noble 2015). It is worth remembering that these
terms were, and continue to be, widely used also by critics of the
gene’s-eye view. For example, the ‘genetic program’ metaphor is
thought to have been independently coined in two papers, one by
François Jacob and Jacques Monod and one by Ernst Mayr (Peluffo
2015). It should also be noted that Bateson described Chapter 2 of
Extended Phenotype as the best rebuttal of genetic determinism he had
ever come across (Bateson 1986; even arch- critic Mary Midgley
described it as ‘admirable’, Midgley 1983). Even so, Bateson argues
that ‘gene-for’-language is slippery. For example, Bateson (1986) criti-
cizes Brian Charlesworth (1978) for referring to a gene ‘coding’ for
altruism. Bateson contends that this implies that there is a one-to-one
correspondence between gene and behaviour. Thus, even the most
careful of population geneticists may appear as if they forgot that they
are dealing with a shorthand.
In general, Bateson thought that gene selectionists’ focus on how
replicators use bodies to produce copies of themselves gives too much
credit to genes in the developmental process. In a classic paragraph in
his review of The Selfish Gene he wrote:
A legitimate focus on gene’s intentions should not be used as an excuse

for resuscitating moribund preformationism. (. . .) Dawkins accepts all
this but then reveals his uncertainty about which language he is using
by immediately giving special status back to the gene as the program-
mer. Consider a case in which the ambient environmental temperature
during development is crucial for the expression of a particular
phenotype. If the temperature changes by a few degrees the survival
machine is beaten by another one. Would not that give as much status
to a necessary temperature value as to a necessary gene? The tempera-
ture value is also required for the expression of a particular phenotype.
It is also stable (within limits) from one generation to the next. It may
even be transmitted from one generation to the next if the survival
machine makes a nest for its offspring. Indeed, using Dawkins’ own
style of teleological argument one could claim that the bird is the nest’s
way of making another nest. (Bateson 1978; my emphasis)
Dawkins first response to Bateson channelling his inner Samuel Butler

was to argue that the nest analogy fails (Dawkins 1978). Nests are not
replicators, as a mutation in the nest—‘for example the accidental
incorporation of a pine needle instead of the usual grass’—is not
transmitted to offsprings’ nests. In other words, whereas one can
plausibly talk about a causal arrow between gene and bird, there is
none in the reverse direction. While true, this was not really Bateson’s
point, which Dawkins would later acknowledge (Dawkins 1982a, p. 98).
Again, this is partly a matter of what aspect of the biology one is
interested in. Whereas development requires biologists to pay equal
attention to both genetic and environmental factors, proponents of
the gene’s-eye view have argued that the unit of selection question
does not, as only genes are replicated and transmitted across gener
ations. Dawkins makes this point with the following backhanded
compliment:
As is so often the case, an apparent disagreement turns out to be due

to mutual misunderstanding. I thought Bateson was denying proper
respect to the Immortal Replicator. Bateson thought that I was denying
proper respect to the Great Nexus of complex causal factors interact-
ing in development. (Dawkins 1982a, p. 99)
The Bateson–Dawkins sparring would continue some three decades

later. Discussing the revived interest in epigenetics, Dawkins sum-
marized the focus on such developmental details as an ‘obscurantist
red herring’ (Dawkins 2004b). He also retold a story of how his
Oxford graduate students used to describe members of Bateson’s
Cambridge department as being adherents to the dictum: ‘Never use
a simple explanation if a more complicated one will do instead.’ As
Bateson admits, this dictum had self-mockingly been endorsed by the
Sub-Department of Animal Behaviour at Cambridge in honour of its
doyen Robert Hinde, who was known to repeatedly emphasize that
‘Behaviour is complicated’ (Bateson 2006a, 2006b). In return, Bateson

offered The Oxford Principle: ‘Never use a causal explanation if a
teleological one will do instead’ (Bateson 2006a). Bateson’s point was
that while the intentional language may be a powerful heuristic, it is
much easier to come up with explanatory stories, which may or may
not be true, than Dawkins acknowledges. Behaviour is complicated
and a one-sided focus on genes misses this.
3.5.1 Evo-devo and developmental systems theory

Whether a focus on genes as the unique bearers of heredity is still
tenable is a hotly contested question in contemporary evolutionary
biology. Bateson is far from the only one who has argued that the
gene’s-eye view, and indeed the broader field of evolutionary biol-
ogy since the modern synthesis, has paid too little attention to devel-
opmental biology and related concepts (see, e.g., Jablonka and
Lamb 2005 and Bonduriansky and Day 2018).
The developmental charge has been organized under two main
labels: evolutionary developmental biology (evo-devo) and develop-
mental systems theory. While proponents of both evo-devo (Müller
2007; Carroll 2008) and developmental systems theory (Oyama 1985;
Ford and Lerner 1992; Gray 1994, 2001; Griffiths and Gray 1994) have
criticized gene-centred approaches to biology using a combination of
empirical and conceptual claims, the latter have done so in a more
radical way. To what extent this is a consequence of evo-devo growing
out of biology and developmental systems theory out of philosophy,
as suggested by Robert et al. (2001), I am not sure. Nevertheless, per-
haps because of its more radical nature, developmental systems theory
has engaged more directly with the conceptual assumptions and
implications of the gene’s-eye view.
The central claim of developmental systems theory is that genes are
not causally special; they do not have a privileged role during devel-
opment. The notion at the heart of this critique is that offspring
inherit more than genes from their parents, including but not limited
to methylation patterns, gut microbes, other contributions from

maternal diet, and ecological habitats, none of which can be said to be
more important than others. Organisms are no more vehicles for rep-
licators than they are for language or other things. This is sometimes
known as the ‘parity argument’, following Susan Oyama’s very
influential book The Ontogeny of Information (Oyama 1985). By this
argument, the fundamental unit of evolution is not the gene but the
life cycle, and the developmental system is the matrix containing all
the resources needed to reproduce the life cycle.
By the term ontogeny of information, Oyama takes aim at the
gene’s-eye view gene as a package of information, not a scrap of
nucleic acid. As Williams noted:‘The gene is a package of information,
not an object. The pattern of base pairs in a DNA molecule specifies
the gene. But the DNA molecule is the medium, it’s not the message’
(Williams 1996b). According to Williams, what is passed on from one
generation to the next is information for how the organism should
develop. In contrast, Oyama posits that this information is reconstructed
during development every generation. To make sense of Oyama’s
point, Sterelny and Griffiths suggested an analogy of a rat memorizing
how to solve a maze (Sterelny and Griffiths 1999, p. 101). Instead of
having the correct route carefully marked out on a map in their brain,
the rat relies on cues from the external environment, such as the
structure of the maze, combined with trees of memories from previ-
ous attempts of solving the maze, to reconstruct the route. T he key is
that the route information is reconstructed every time, not passed on
intact. In the same way, Oyama argued, embryonic development does
not rely on a filled out developmental programme—there is no
preformed plan—but genes interact with other informational sources
within and outside the embryo itself.
Developmental system theorists also reject the standard nature ver-
sus nurture dichotomy. Their argument is not just that most traits are
the product of both, as well as their interaction. That, no one disputes.
Rather, they argue that it leads to the wrong questions being asked
(Griffiths and Taberny 2013). In Chapter 1, I argued that Fisher’s paper
‘The correlation between relatives on the supposition of Mendelian

inheritance’ (Fisher 1918) marked the beginning of the gene’s-eye
view, partly thanks to his introduction of the concept of variance.
Fisher and subsequent researchers used this idea to ask how much dif-
ference in a trait among individuals in a population was attributable
to genetic differences and how much was due to environmental dif-
ferences. To developmental system theorists, this dichotomous view
of nature and nurture results in an unproductive focus on how much
rather than how development unfolds.
The interest that developmental systems theorists have shown in
the gene’s-eye view appears not to have been reciprocated by gene
selectionists. One exception is Sterelny et al. (1996), who argued that
by extending the replicator concept, one could incorporate most
insights from developmental systems theory within the replicator-
vehicle framework (see Lu and Bourrat 2018 for a similar argument
and Griffiths and Gray 1997 for a reply). While it is important to
explore how different frameworks can be integrated, it is not always
crucial that they are. Just as I agree with Maynard Smith’s discussion
of different ways of modelling social evolution outlined above, I share
much of Haig’s assessment that developmental systems theory is logically
coherent and likely a more suitable heuristic framework for certain
questions in biology than the genic perspective (Haig 2012).
3.6 Human nature and human affairs
In a letter to his good friend, the botanist Joseph Dalton Hooker, written
15 years before the publication of The Origin of Species, Darwin described
his feelings concerning his theory of evolution like ‘confessing a murder’
(Darwin Correspondence Project 2020c). T he implications of Darwin’s
theory for science, philosophy, and religion were huge (Ruse 1986;
Dennett 1995; Sober 2011).As Darwin jotted down in a notebook in 1838:
‘Origin of man now proved. Metaphysic must flourish. He who under-
stands baboon would do more towards metaphysics than Locke’
(Darwin 1838).
Evolutionary biology has had a rocky relationship with the concept

of human nature and human affairs ever since. On page 1 of The
Selfish Gene, Dawkins approvingly quotes George Gaylord Simpsons
comment that all attempts to answer the question ‘what is man?’ prior
to 1859 were ‘useless’ and ‘best ignored’. T
he anthropologist Marshall
Sahlins could not have disagreed more. In his The Use and Abuse of
Biology: An Anthropological Critique of Sociobiology, he wrote of evolu-
tionary approaches to human behaviour as contributing ‘primarily to
the final translation of natural selection into social exploitation’
(Sahlins 1976, p. 73).
Central to these disparate opinions was the issue of genetic
determinism. As Lewontin, Rose, and Kamin put it in Not in Our
Genes:
Sociobiology is a reductionist, biological determinist explanation of

human existence. (. . .) The academic and popular appeal of sociobiol-
ogy flows directly from its simple reductionist program and its claim
that human society as we know it is both inevitable and the result of
an adaptive process. (Lewontin, Rose and Kamin 1984, p. 236).
A few years earlier, in the winter of 1981, Rose had written to Nature
to alert readers of an article in New Nation, a magazine associated with
the UK far-right organization National Front, titled ‘Nationalism,
racialism: products of our selfish genes’ (Rose 1981). The article
included a photo of Dawkins and cited the works of Dawkins,
E.O. Wilson, Maynard Smith, and one ‘Travers’ (which, Rose points
out, presumably was meant to be Trivers) as bolstering their white
supremacy position. Rose’s letter ended with the following appeal:
‘May I suggest that it would be in the public interest that John
Maynard Smith and Richard Dawkins should clearly dissociate
themselves from the use of their names in support of this neo-Nazi
balderdash’ (Rose 1981). Dawkins (1981b) and Maynard Smith (1981)
both promptly, and without hesitation, did just that, saying that ‘there
is nothing in modern evolutionary biology which leads to that
conclusion [that our genetic constitution makes it impossible for us to
live in a racially integrated society]’ (Maynard Smith 1981). T his was
not the first time that Rose had made Maynard Smith publicly distance
himself from the misrepresentations of his work. A year and a half
earlier, in June 1979, Maynard Smith had typed a letter to New Scientist
that the editors gave the title ‘Thatcher’s biology’:
When, in 1964, I wrote a largely mathematical paper in Nature on
‘Group and kin selection’ I did not know that I was starting a chain of
events that would lead to the election of Mrs Thatcher’s government.
Indeed, I only realised it when I read Steven Rose’s ‘The Thatcher view
of human nature’ (Forum, 18 May, p 575). I yield to no one, not even
to Rose, in my dislike of Mrs Thatcher’s declared policies, but what
would he have me do? Fiddle the algebra? (Maynard Smith 1979)
As discussed earlier, the charge of genetic determinism is largely

unfair.While proponents of the gene’s-eye view may assign too much
causal power to genes, they are not denying a role of the environment.
Genes are difference makers, but that does not mean that only genes
matter (as Bateson noted, any doubters should consult chapter 2 in
The Extended Phenotype).Yet, several other books on this theme were
published around the same time. Examples included Against Biological
Determinism (Rose 1982a), Towards a Liberatory Biology (Rose 1982b),
and The Dialectical Biologist (Levins and Lewontin 1985). However, it
was Not in Our Genes that made Dawkins ‘stand up and be counted’
as a sociobiologist, something he had resisted due to his dislike of the
term (Dawkins 1985; see also Dawkins 1986b). T he many ins and outs
of this historical period are covered in an excellent, comprehensive
way in Ullica Segerstrale’s Defenders of the Truth:The Sociobiology Debate
(Segerstrale 2000). Here, I will focus on one specific implication of
evolutionary biology in general and the gene’s-eye view in particular:
is the universe naturally good or bad or indifferent?
3.6.1 T.H. Huxley and Darwinian nightmares

Upon reading The Selfish Gene, Randolph Nesse—one of the founders
of the field of evolutionary medicine and co-author with George
Williams of Why We Get Sick: The New Science of Darwinian Medicine
(Nesse and Williams 1994)—described how it left him with weeks of

dreaming about lumbering robots (Nesse 2006). He was not alone. In
the preface of Unweaving the Rainbow, Dawkins describes how a
foreign publisher could not sleep for three days after reading The
Selfish Gene, he was so disturbed by what he considered to be the cold
and bleak implications of the book (Dawkins 1998b, p. ix). What were
these implications?
The Selfish Gene is not especially concerned with humans, a point
lost on many commentators on moral matters (but see Williams 1976
for an exception). On this issue Dawkins clearly differs from
E.O. Wilson, who followed Sociobiology with On Human Nature, a
book that explicitly deals with how sociobiology applies to humans
(Wilson 1978). Instead, the bleakness that so many readers found so
repugnant came from a more general view of the universe. In River
Out of Eden Dawkins writes that ‘a universe of electrons and selfish
genes, blind physical forces and genetic replication (. . .) has precisely
the properties we should expect if there is, at bottom, no design,
no purpose, no evil, no good, nothing but pitiless indifference’
(Dawkins 1995b, p. 133). Similarly, in A Devil’s Chaplain he writes that
‘Blindness to suffering is an inherent consequence of natural selec-
tion. Nature is neither kind nor cruel but indifferent’ (Dawkins 2003,
p. 9). T
he title itself comes from another letter from Darwin to Hooker,
in which he wrote:‘What a book a devil’s chaplain might write on the
clumsy, wasteful, blundering low and horridly cruel works of nature!’
(Darwin Correspondence Project 2020d).
Williams’s views were along the same lines. He described mother
nature as a ‘wicked old witch’ and considered natural selection to be
‘a morally unacceptable process’ (Williams 1993) that could ‘honestly
be described as a process for maximizing short-sighted selfishness’
(Williams 1989). For this reason, both Williams and Dawkins were also
highly critical of the Gaia hypothesis (Lovelock and Margulis 1974;
Lovelock 1979). T he Gaia hypothesis is the idea that Earth and its liv-
ing organisms interact in a synergistic self-regulating way in order to
maintain life and is sometimes seen as alternative conception of the
world, a more romantic one, focused less on conflict and competition

and more on cooperation and harmony.Williams and Dawkins force-
fully argued that it contradicted evolutionary theory (e.g. Dawkins
1982a, pp. 234–237; Williams 1993).
Dawkins and Williams were not the first to make the case that the
world is a ruthless place. The phrase ‘nature red in tooth and claw’
appeared in Lord Tennyson’s poem ‘In Memoriam A.H.H.’ in 1850, a
message Dawkins (1976, p. 2) and Williams (1989) both endorsed as
providing an accurate summary of the modern understanding of
natural selection. More than Lord Tennyson, however, T.H. Huxley
was the premier spokesperson for this world view. Mary Midgley even
went so far as to call Dawkins a ‘Huxleyean rather than a Darwinian
thinker’ (Midgley 2010, p. 47). Given that Dawkins is often accused of
being a naive adaptationist, the moniker is a little strange. As noted in
Chapter 1, Huxley had serious doubts about the power of natural
selection and was not particularly impressed by adaptations.
Furthermore, the influence of Huxley was probably even greater on
Williams. After all, he co-edited a new edition on Huxley’s celebrated
Romanes Lectures, Evolution and Ethics, delivered in Oxford in 1892
and published 2 years later (Paradis and Williams 1989).While Huxley
and contemporary Social Darwinists like Herbert Spencer shared a
generally Hobbesian view of nature as being ‘on about the same level
as a gladiator show’ (Huxley 1888, p. 200), he firmly rejected the
implication that this is how it therefore should be. Instead, as he
argued in his Romanes lecture, the natural process needs to be defeated:
‘Let us understand, once for all, that the ethical progress of society
depends, not on imitating the cosmic process, still less in running
away from it, but in combating it.’ (Huxley 1894, p. 83). Williams
strongly approved of Huxley’s message:
With what other than condemnation is a person with any moral sense
supposed to respond to a system in which the ultimate purpose in life
is to be better than your neighbor at getting genes into future gener
ations, in which those successful genes provide the message that instructs
the development of the next generation, in which that message is
always ‘exploit your environment, including your friends and relatives,

so as to maximize our genes’ success, in which the closest thing to a
golden rule is ‘don’t cheat, unless it is likely to provide a net benefit’?
(Williams 1997, p. 154)
Someone who did not care much for Huxley’s message was the
Russian aristocrat, anarchist, and scientist Peter Kropotkin. Outraged
by Huxley’s ‘The struggle for existence in human society’ quoted
above (Huxley 1888), Kropotkin developed his argument in eight
essays during the 1890s, eventually jointly published in Mutual Aid: A
Factor of Evolution (Kropotkin 1902). Relying primarily on his own
fieldwork in the remote parts of Siberia, Kropotkin’s central thesis was
that relationships among organisms were best characterized, not by a
struggle for existence, but by mutual solidarity. Making sense of
Huxley and Kropotkin and the broader connection between evolu-
tionary theory and ethics is far from trivial (see extensive treatments
by, e.g., Rachels 1991; Nitecki and Nitecki 1993; James 2010).
Like Kropotkin, several modern writers have also sought to state
the case that the world is not fundamentally selfish. Books making this
argument have often used variations on the title of The Selfish Gene to
make the point. Examples include Joachim Bauer’s Das kooperative
Gen: Abschied vom Darwinismus (The Cooperative Gene: Farewell
to Darwinism; Bauer 2008), Joan Roughgarden’s The Genial Gene
(Roughgarden 2009), Fern Elsdon-Baker’s The Selfish Genius (Elsdon-
Baker 2009), and Göran Greider’s Den solidariska genen (The Loyal
Gene; Greider 2014). In fairness, books supportive of a gene’s-eye
view have had similar titles. One example is Dawkins’s former student,
Mark Ridley’s Mendel’s Demon: Gene Justice and the Complexity of Life
(Ridley 2000), which was renamed The Cooperative Gene: How Mendel’s
Demon Explains the Evolution of Complex Beings for the American
market.
Others have also worried about the association between selfish
genes and selfish humans. Andrew Briggs, Hans Halvorson, and
Andrew Steane suggest replacing ‘selfish genes’ with ‘eager genes’
simply because the latter is ‘morally neutral’ (Briggs et al. 2018,
pp. 201–202). Another example is the group selection advocate David

Sloan Wilson, who has argued that the gene’s-eye view (as well as
inclusive fitness and game theory) is simply a way to transform altru-
ism into selfishness (Wilson 2015a, p. 32). Finally, Roughgarden (no
friend of group selection) has described orthodox sexual selection
theory, which she places in the same intellectual camp as the gene’s-
eye view under the label ‘neo-Spencerism’ (from Herbert Spencer), as
being underwritten by ‘genetic classicism’ and ‘genetic entitlement’
(Roughgarden 2009, p. 4). Further, she argues that ‘if sexual selection
is indeed true, then so be it; and the prospect of an egalitarian society
is an unrealistic mirage’ (Roughgarden 2009, p. 5).
To me, there is no better response to these worries than the one
developed by David Hume and G.E. Moore. In a short paragraph in
A Treatise of Human Nature, Hume argued that you cannot coherently
move from a statement about how the world is to a statement about
how the world ought to be (Hume 1793, Book III, Part I, Section I).
A century later, Moore developed a similar idea in Principia Ethica and
coined the term naturalistic fallacy to refer to the mistake (Moore 1903).
Dawkins was very much on the same page as Huxley and Williams, as
well as Hume and Moore. Discussing the prospect of going from evo-
lution to ethics he stated:
As an academic scientist I am a passionate Darwinian, believing that
natural selection is, if not the only driving force in evolution, certainly
the only known force capable of producing the illusion of purpose
which so strikes all who contemplate nature. But at the same time as
I support Darwinism as a scientist, I am a passionate anti-Darwinian
when it comes to politics and how we should conduct our human affairs.’
(Dawkins 2003, pp. 10–11)
Indeed, Dawkins ends the first edition of The Selfish Gene with:
We have the power to defy the selfish genes of our birth and, if neces-
sary, the selfish memes of our indoctrination. (. . .) We are built as gene
machines and cultured as meme machines, but we have the power to
turn against our creators. We, alone on earth, can rebel against the
tyranny of the selfish replicators. (Dawkins 1976, p. 215)
The way we talk about evolution has ramifications for how we view
ourselves.Yet, just as there is no contradiction in the physician scientist
devoting her career to both describing and eradicating cancer, our
commitment to the science of evolution says nothing about our moral
outlook. Selfish genes do not necessarily make selfish people.
3.7 Summary
• Anthropomorphizing is a much- maligned concept in biology,

but when paired with mathematical modelling (licensed anthropo-
morphizing) it can be a very powerful thinking tool.
• While the gene’s-eye view is most straightforward under additivity,
complex genetic interactions, such as epistasis, dominance, or het-
erozygote advantage, are not as big a problem as some critics make
them out to be.
• The bookkeeping objection is one of the most famous criticism of
the gene’s-eye view. It holds that while all evolutionary change can
be recorded as changes in allele frequencies, it is incorrect to there-
fore assign causality to the level of genes. Disagreements over the
merit of this objection to the gene’s-eye view led to a fertile philo-
sophical debate over pluralism in evolutionary explanations.
• Developmental biologists have long been critical of what they per-
ceive as the gene’s-eye view’s overly narrow focus on genes’ causal
primacy in development. The most ambitious form of this critique
has been organized as developmental systems theory, which offers a
radically different approach to biology that also has heuristic value.
• The gene’s-eye view was also entangled in debates over human
nature. Both Williams and Dawkins express a rather bleak Huxleyan
view on the universe and agreed that it is up to us to be the good
we want to see in the world.
4
Inclusive Fitness and
Hamilton’s Rule
4.1 Introduction
T o explain what was so special about her mentor W.D. (Bill)

Hamilton, Marlene Zuk wrote that the difference between him
and everyone else was ‘not the quality of his ideas, but their sheer
abundance’ (Zuk 2000). The proportion of his ideas that were actually
any good was about the same as anyone else, instead:
the difference between Bill and most other people was that he had a
total of over one hundred ideas, with the result that at least ten of them
were brilliant, whereas the rest of us have only four or five ideas as long
as we live, with the result that none of them are. (Zuk 2000)
Hamilton indeed had number of brilliant ideas. He made substantial

contributions to the study of the origin of sex, sex ratios, genomic
conflicts, host–parasite interactions, and the evolution of senescence
(Grafen 2004; Segerstrale 2013). His most influential idea, and the one
that bears his name, is about the evolution of social behaviour, espe-
cially altruism and showed that it is possible to evolve social behaviour
that comes with a fitness cost if the beneficiary of that behaviour is a
relative (Hamilton’s Rule).
Many are the biology students who first learned about the intrica-
cies of Hamilton’s work through the writings of Dawkins. The first
DOI: 10.1093/oso/9780198862260.003.0005
I nclusi v e f itn ess a n d H a m i lton’s Ru le 117
draft of The Selfish Gene was based on a series of lecture notes Dawkins
developed to communicate Hamilton’s ideas to his undergraduate
students (Dawkins 2013a, p. 201). One of these former students, Jim
Mallett, now a professor at Harvard University and University College
London, recalls the name of the course to have been ‘Gene Machines’
( J. Mallet, personal communication). T he course title later inspired
the name of Chapter 4 of The Selfish Gene (The gene machine).
If Dawkins clearly cherished teaching, especially within the Oxford
tutorial system (Dawkins 2008a), Hamilton had a different reputation.
He was a notoriously bad lecturer, at least as far as large undergraduate
courses went. During his time as a junior faculty member at Imperial
College, Silwood Park, undergraduates used to urge the departmental
administrators not to count their results in Hamilton’s course towards
their degree marks (Segerstrale 2013, p. 392). Robert Trivers also recalls
Hamilton coming to give a talk at Harvard only to deliver ‘one of the
worst lectures [Trivers] had ever seen in [his] life’ (Trivers 2015, p. 188).
Many biologists therefore seem to have learned about Hamilton’s
work from secondary sources. T he fact that Hamilton’s two-part
landmark paper from 1964 (Hamilton 1964a, 1964b) has often been
cited incorrectly has been taken as evidence of this. The correct title
is ‘The genetical evolution of social behaviour’ but, as Seger and
Harvey (1980) showed, out of 200 papers published between 1965 and
1979 some 20% cited it as ‘The genetical theory of social behaviour’
instead. The paper was miscited by all sorts of authors, critics and sup-
porters alike, and among graduate students as well as luminaries
including Stephen Jay Gould, Richard Lewontin, E.O. Wilson, and
John Maynard Smith. Seger and Harvey noted that among the sixty-
three papers published before 1975 only one contained the incorrect
citation, leading them to suggest that many had used the erroneous
version found in the first edition of E.O. Wilson’s Sociobiology
(Wilson 1975). T he first edition of The Selfish Gene also contains this
mistake, and whether the error came from either book or not is
unclear. In the endnotes added to the second edition of The Selfish
Gene published in 1989, Dawkins devotes quite a bit of space to
rebutting what he considers to be a ‘memetic myth’ (Dawkins 1989,

p. 326). T
he mutant title, Dawkins argues, is just one word off and its
similarity to Fisher’s The Genetical Theory of Natural Selection makes
multiple independent errors quite likely.
Dawkins was also instrumental in rectifying public misunderstand-
ings of Hamilton’s work. One good example is his ‘Twelve misunder-
standings of kin selection’ (Dawkins 1979). In it, he outlined and
refuted common mistakes other researchers had made in print. For
example, misunderstanding number 3 was ‘The theory of kin selec-
tion demands formidable feats of cognitive reasoning by animals’. An
example of this came from the earlier mentioned The Use and Abuse
of Biology, where Marshall Sahlins wrote of the ‘considerable mysti-
cism’ involved in Hamilton’s work:
In passing it needs to be remarked that the epistemological problems

presented by a lack of linguistic support for calculating, r, coefficients
of relationship, amount to a serious defect in the theory of kin selec-
tion. Fractions are of very rare occurrence in the world’s languages,
appearing in Indo-European and in the archaic civilizations of the
Near and Far East, but they are generally lacking among the so-called
primitive peoples. Hunters and gatherers generally do not have count-
ing systems beyond one, two and three. I refrain from comment on the
even greater problem of how animals are supposed to figure out how
that r (ego, first cousins) = 1/8. (Sahlins 1977, pp. 44–45).
In response, Dawkins wryly asked where, given the logarithmic spiral

of its shell, a snail was meant to keep its log tables? Some of the listed
misunderstandings may seem a little silly when read today. Nevertheless,
they do persist. Take, for example, misunderstanding number 5: ‘All
members of a species share more than 99% of their genes, so why
shouldn’t selection favour universal altruism?’ This seems to have to
have originated with Washburn (1978) but was perpetuated as late as
2004 by Niles Eldredge (in a book with the subtitle ‘Rethinking sex
and selfish genes’, to boot; Eldredge 2004, pp. 42–43).
There is thus a long and intimate association between the gene’s-
eye view and the concept of inclusive fitness and Hamilton’s Rule. In
this chapter, I examine that relationship. I first introduce what I call

Hamilton’s unfinished revolution. Hamilton provided one of the first
clear articulations of the gene’s-eye view but, much to the frustrations
to the likes of Dawkins and Maynard Smith, never completely
switched to a fully gene-centric approach. More generally, proponents
of the gene’s-eye view and inclusive fitness have emphasized their
equivalence, while also stressing the limitations of the other. T he
connection between the two is partly a product of personal connec-
tions between key individuals involved, but there is also a more formal
link. To demonstrate this, I outline a derivation of the so- called
general version of Hamilton’s Rule, which looks rather different
from the informal version (rb > c) that makes an appearance in most
introductory evolution courses. This general version is also at the
centre of much of the current kerfuffle over Hamilton’s work and I
explain why this is and how the gene’s-eye view fits into those
debates.
Central to many disagreements over inclusive fitness is the issue of
how to scientifically handle the neo-Paleyan fascination with the
appearance of design that is such a key motivator for both the gene’s-
eye view and inclusive fitness theory. One attempt is Alan Grafen’s
ambitious Formal Darwinism Project, which seeks to construct a
mathematical bridge between the dynamics of population genetics
and the appearance of design. I discuss how this project provides an
interesting window into the relationship between the gene’s-eye view
and inclusive fitness. In particular, Grafen’s solution—that organisms
should behave as if designed to maximize their inclusive fitness—
highlights the need for unity of purpose among genes. How to handle
what happens when this unity breaks down (when genes are in con-
flict) and strikes at core of the connection between genic and the
organismic approaches.
Examinations of the relationships between the gene’s-eye view and
inclusive fitness continue to this day. I end the chapter by discussing
two recent attempts at reconciling insights from the two perspectives
and what light these arguments can shed on the gene’s-eye view.
4.2 The origin and diversity of Hamilton’s Rule
Hamilton’s life in biology began at the University of Cambridge.

While there, he discovered R.A. Fisher; first by finding The Genetical
Theory of Natural Selection in the library and later the man himself,
then a retired professor in the Genetics Department. T he effect that
The Genetical Theory had on the young Hamilton is almost impossible
to exaggerate. One need only read Hamilton’s endorsement on the
back of the 1999 Complete Variorum Edition of the book:
This is a book which, as a student, I weighed as of equal importance to
the entire rest of my undergraduate Cambridge BA course and, through
the time I spent on it, I think it notched down my degree. Most chap-
ters took me weeks, some months; even Kafka whom I read at the
same time couldn’t depress me like Fisher could on say, the subject of
charity, nor excite me like his theory of civilization. T errify was even
the word in some topics and it still is, so deep has been the change
from all I was thinking before. (…) By the time of my ultimate gradu-
ation, will I have understood all that is true in this book and will I get
a First? [the highest level of degree a UK undergraduate can receive]
I doubt it. In some ways some of us have overtaken Fisher; in many,
however, this brilliant, daring man is still far in front. (Hamilton 1999)
Reading Fisher not only cemented Hamilton’s interest in evolution

but also planted the seed of what would be his obsession for the early
years of his career: the genetics of altruism. After Cambridge, he
moved to London for his graduate research, but his time in the capital
appears to have been miserable. He was often so lonely that he lin-
gered in underground stations and public buses in order to receive
some human interactions (Segerstrale 2013, p. 64). Still, by any stand-
ard, his PhD work has had far-reaching influence. On 7th March
1963, he wrote to Colin Hudson, his close friend from their Cambridge
undergraduate days, telling him that: ‘My “letter” has been accepted
by the “American Naturalist”, which is very encouraging (…) I am
still working on the last section of my main paper—the real manifesto’
(Reprinted in Segerstrale 2013, p. 85). The ‘letter’ would appear as ‘The
evolution of altruistic behavior’ later the same year. T owards the end
of his career, Hamilton would refer to the paper as his ‘little-read first
paper’ (Hamilton 1996, p. 5). He had actually completed ‘the real man-
ifesto’ prior to penning his letter, but a reviewer (who we now know
was John Maynard Smith) had suggested extensive rewrites, including
splitting the paper into two (hence, Hamilton 1964a, 1964b). Feeling
the pressure from his graduate advisors, he decided to submit a short
précis of his key ideas. After a rapid desk rejection from Nature—
which was accompanied with the advice to try a ’psychological or
socialogical [sic] journal’ (Hamilton 1996, p. 3)—he decided to send
the ‘letter’ to the American Naturalist.
Despite being less than three pages long, the paper is remarkably
full of novel insights (Gardner 2015; Marshall 2015, pp. 11–13). For
instance, the paper contains one of the clearest and earliest articula-
tions of the gene’s-eye view. Discussing a locus where the G allele
causes its carrier to perform some sort of altruistic behaviour, whereas
g has no such effect, he writes:
Despite the principle of ‘survival of the fittest’ the ultimate criterion

that determines whether G will spread is not whether the behavior is
to the benefit of the behaver but whether it is of benefit to the gene
G (…) With altruism this will happen only if the affected individual is
a relative of the altruist, therefore having an increased chance of carry-
ing the gene, and if the advantage conferred is large enough compared
to the disadvantage to offset the regression, or ‘dilution,’ of the altruist’s
genotype in the relative in question. (Hamilton 1963)
In only a few sentences, Hamilton presents the profound insight that

from a gene’s point of view it does not matter if you are transmitted
through the body in which you reside, or through a copy of yourself
that is present in another individual. To capture this insight quantita-
tively, he introduced the inequality
k > 1/ r
where k is the ratio of fitness benefit to recipient and fitness cost to
actor and r the degree of relatedness. This simple expression describes
the necessary and sufficient conditions for a gene to be favoured by

natural selection. Now known as Hamilton’s Rule, a term first coined
by Charnov (1977), it is usually expressed in the simpler form rb > c,
where r is still the degree of relatedness, and b is the benefit to the
recipient and c is the cost to the actor.
Hamilton considered his work an ‘extension of the classical theory’
of natural selection (a coy reference to the poor reputation of Fisher’s
Fundamental Theorem; Hamilton 1963). In addition to Hamilton’s
Rule, the key part of this extension was the concept of inclusive fit-
ness. The following year, in 1964, in the majestic two-part paper for
The Journal of Theoretical Biology. Hamilton defined it thus:
Inclusive fitness may be imagined as the personal fitness which an

individual actually expresses in its production of adult offspring as it
becomes after it has been first stripped and then augmented in a cer-
tain way. It is stripped of all components which can be considered as
due to the individual’s social environment, leaving the fitness which he
would express if not exposed to any of the harms or benefits of that
environment. This quantity is then augmented by certain fractions of
the quantities of harm and benefit which the individual himself causes
to the fitnesses of his neighbors. T he fractions in question are simply
the coefficients of relationship appropriate to the neighbours whom
he affects. (Hamilton 1964a)
More informally it can be summarized as:
Inclusive fitness = direct fitness + indirect fitness
To calculate an individual’s inclusive fitness you first determine its direct

fitness, to which you add those parts of the fitnesses of others for which
the focal individual is causally responsible (scaled by relatedness; the
indirect fitness). Finally, you then subtract (‘strip’) the part of the personal
fitness that is due to the social environment of the focal individual.
The last stripping step is to avoid the same fitness being counted
twice, both as the focal individual’s and that of a social partner, as if a
given offspring had multiple existences (so-called double counting;
Grafen 1982; Queller 1996; see also Levin et al 2019 for a recent
example of how to handle this issue in practice). Because the pheno-

types of relatives are correlated due their shared ancestry, this subtrac-
tion is essential in order to properly separate causal from correlational
effects. By ignoring fitness effects due to actions beyond the focal
individual, it also keeps inclusive fitness under the full control of the
individual.
The central message here is that an individual organism may caus-
ally affect the transmission of a given gene both through having off-
spring on its own and by helping relatives increase their reproductive
success. As shown by Hamilton, depending on preferences, this pro-
cess can be captured either from the perspective of an individual
organism by using inclusive fitness or from a gene’s-eye view. Crucially,
Hamilton considered inclusive fitness to be a causal property of the
individual organism, a fact that will become relevant later on.
In addition to Hamilton’s Rule and inclusive fitness, the third term
to come out of Hamilton’s work on social evolution is kin selection.
Not a term coined by Hamilton himself, but by Maynard Smith
(1964), kin selection is selection involving interactions among genea-
logical kin. Kin selection has been less controversial than its two sister
concepts, likely a consequence of it being an empirical process, rather
than a mathematical framework (Birch 2017a). As will become clear,
the mathematical properties of Hamilton’s Rule and inclusive fitness
leave much room for disagreements.
4.2.1 Hamilton’s Rule today

Hamilton’s Rule and inclusive fitness were criticized from the get-go.
Theoretical population geneticists, who saw little value in the concept
compared to more exact modelling approaches were especially crit
ical (examples included Cavalli-Sforza and Feldman 1978; Feldman
and Cavalli-Sforza 1981; Karlin and Matessi 1983). T he beginning of
the most recent iteration of the debate is usually dated to the publica-
tion of a paper titled ‘The evolution of eusociality’ in Nature, by
E.O. Wilson and two mathematicians turned mathematical biologists,
Corina Tarnita and Martin Nowak (Nowak et al. 2010). T he paper led

to a flurry of back-and-forth argument and counter-arguments (see,
e.g., Abbott et al. 2011; Gardner et al. 2011; Allen et al. 2013;
Marshall 2015; Liao et al. 2015; Nowak and Allen 2015; van Veelen
et al. 2017 for some of the original arguments; and Birch 2014, 2017a,
2017b, Birch and Okasha 2015 for overviews).
The current controversy can be illustrated by contrasting state-
ments from leading authors on each side of the debate. One the one
hand, in the paper that kicked off the recent spat, Nowak et al. state
that Hamilton’s Rule ‘almost never holds’. On the other hand, 137
authors described Nowak et al.’s statement as ‘based on a misunder-
standing of evolutionary theory and a misrepresentation of the empir-
ical literature’ (Abbot et al. 2011). Similarly, Gardner et al. (2011)
characterized it as ‘simply incorrect’ and go on to argue that Hamilton’s
Rule has ‘the same generality and explanatory power as the theory of
natural selection itself ’. To see why the tone has become so derisive,
it is instructive to go through the assumptions of the contested ver-
sion of Hamilton’s Rule, the so-called general version. These assump-
tions are what make the version so attractive for its supporters and so
unbearable for its critics (Box 4.1).
The criticism stemming from Nowak et al. (2010) of the general
version of Hamilton’s Rule stands on three legs (Birch 2017b,
pp. 64–76): it is tautological, it makes no predictions, and it fails to
generate causal explanations. Crucial to all arguments are the minimal
assumptions involved in deriving it. In fact, in one articulation of this
criticism, Allen et al. (2013) go so far as claiming that it requires no
assumptions. This is not quite true. Take, for example, Queller’s deci-
sion to drop E ( w i D pi ) (Box 4.1). Because of phenomena such as self-
ish genetic elements, genetic transmission will be biased more often
than many biologists probably appreciate, and E ( w i D pi ) will thus not
equal 0. At the same time, the importance of selfish genetic elements
is hardly at the heart of the disagreement between proponents and
critics of Hamilton’s Rule, so the relevance of this particular fact is
somewhat limited. Nevertheless, a model is only ever as good as its
Box 4.1 The general version of Hamilton’s Rule

The version of Hamilton’s Rule at the heart of the disagreement takes
a little getting used to.This way to capture Hamilton’s Rule, sometimes
referred to as the ‘general model’ as it is more general than Hamilton’s
own derivation, was developed by David Queller in the early 1990s
(Queller 1992). Queller’s paper is readable also for those of us without
formal training in mathematical theory, but there are also several good
primers on the model (see, e.g., Gardner et al. 2011 and Marshall 2015).
Here, I follow the lead of Jonathan Birch, whose book The Philosophy
of Social Evolution is a thorough introduction to the many conceptual
issues underlying disagreements in social evolution research, especially
those stemming from Hamilton’s work (Birch 2017b).
Queller’s derivation of Hamilton’s Rule takes its starting point in
the Price equation.The Price equation is an abstract statement about
evolutionary change from one generation to the next (Price 1970;
Frank 2012; Gardner 2020), such that:
1
Dp = [Cov( w i , pi ) + E ( w i D pi )] (1)
w
The change in population frequency of a given allele ( D p ), where
pi is the individual gene frequency of the ith individual for the allele
under consideration, is the sum of two population statistics. The first
is the selection term, given by Cov(wi,pi ), the covariance between
individual fitness wi and individual gene frequency pi. The second is
the transmission term, E ( w i D pi ), the expected change in pi between
parent and offspring. Both terms are weighed by the population
mean fitness w.
With this in place, Queller makes three key assumptions when
deriving Hamilton’s Rule. First, pi is reinterpreted as a breeding
value, as used in quantitative genetics. This is possible because pi
can be thought of as not just an individual gene frequency, but as
a linear combination of frequencies across multiple alleles of
multiple loci. From this, D p becomes the change in a quantitative
polygenic trait.
(Continued )
Box 4.1. (Continued)

Next, the transmission term E ( w i D pi ) is assumed to be 0. This
assumption has two key biological implications. First is that processes
like segregation distortion, gametic selection, and genetic drift are
assumed to be negligible and so safe to ignore. Second is that the average
effects of alleles on the considered phenotype are constant. Because
dominance and epistasis can both cause this assumption to be violated,
the way to make sense of this assumption is to return to Fisher’s
expanded concept of the environment that was introduced in Chapter 1,
which includes the rest of the genome. Both assumptions are quite
substantial and strike at the heart of the relationship between Hamilton’s
Rule and the gene’s-eye view. I will return to them later in the chapter.
Finally, with E ( w i D pi ) dropped, Queller takes Cov(wi,pi ) to be the
effect of natural selection on the evolutionary change of the trait
under study. This leaves:
1
D p = [Cov( w i , pi )] (2)
w
To get from this to the familiar rb > c, the selective covariance term
must be partitioned into rb and c. Queller achieves this by making
use of the Lande–Arnold regression model of fitness (Lande and
Arnold 1983). The fitness of the ith individual can therefore be stated
using a linear regression model, so that:
w i = a + b1 pi + b 2 pˆ i + e wi (3)
Such linear function considers the gene frequency of a given
individual (pi), as well as the average individual’s gene frequency of
its social partners ( pˆ i ) . It then captures the partial regression of an
individual’s fitness on that individual’s gene frequency ( bi ), accounting
for that of the social partners and the partial regression of an individual’s
fitness on the gene frequency of social partners, this time accounting
for that individual’s gene frequency. α is the non-social part of fitness
and taken to be the same for all individuals. e wi is the traditional error
term of linear regressions and here it represents the discrepancy
between actual and predicted fitness of the ith individual.This regression
model is then substituted into the Price equation (2), leading to:
w D p = Cov(a , pi ) + b1Var ( pi ) + b 2Cov( pˆ i , pi ) + Cov(e wi , pi ) (4)
Simplifying and rearranging to state the condition for the

population mean of the trait of interest to increase D p > 0 gives:
Cov( pˆ i , pi )
D pˆ  0 Û b 2  - b1 (5)
Var ( pi )
Then, because r, b, c, in Hamilton’s Rule can be defined as:
Cov( pˆ i , pi )
r= , b = b 2 , and c = - b1
Var ( pi )
this notation means that (5) can be rewritten as:
( D p )  0 Û rb  c
That is, the frequency of a given allele will increase in the
population if and only if rb > c.
This, then, is the general version of Hamilton’ Rule. At this point,
it is worth pausing and reflecting on what the variables in the general
version actually mean. Because there is no such thing as a regression
coefficient for a single data point, r, b, and c are not actually properties
of individual organisms or of any given social interaction (as a verbal
description of Hamilton’s Rule may lead you to believe). Instead,
they are population statistics: r is the slope of the line of best fit
plotting pˆ i against pi for every individual in the population, and b
and c can be calculated from the plane of best fit after adding wi to
the pˆ i against pi plot. This formulation may at first seem strange, but
it leads to a flexibility that can be either a great strength or a great
weakness depending on what you want the model to achieve.
assumptions (garbage in, garbage out, to be crass), and one can argue
that because the assumptions of the general version of Hamilton’s Rule
are so minimal, so are the scientific insights that can be gained from it.
These criticisms are all fair and not to be dismissed lightly. T he
general version of Hamilton’s Rule is in fact of little help in predicting
evolutionary change in a given ecological situation. Even so, rb > c
also offers a really simple framework for empirical workers to use as
starting point, without the need for more sophisticated and specific
models. More exact predictions require further assumptions motiv
ated by the particular biological system modelled. Moreover, because
regression coefficients are used to define the parameters, it can only
ever identify correlations, not actual causations.
There is a sense, however, in which these criticisms measure the
value of the general version of Hamilton’s Rule against the wrong
yardstick. The point of the general version is not to provide exact
fine-grained causal explanations of particular scenarios, but to instead
offer a way to classify, compare, and contrast more detailed causally
appropriate models (the kind that biologists have been making for
decades; Gardner et al. 2007, 2011; Marshall 2015). As an organizing
framework, the general version also offers a way to identify common
mechanisms in the origin of social behaviours. It provides a classifica-
tory scheme and common vocabulary to translate among models,
which allows more detailed theoretical models to be interpreted,
compared, and contrasted in a unified way. Having mathematical
frameworks that themselves make no predictions but facilitate com-
parisons among more specific models is in no way unique to social
evolution. For example, this also is the case in physics, as recently
expressed by Nobel Prize winner Steven Weinberg:‘Our most import
ant theories, like Newtonian mechanics and quantum mechanics, are
not falsifiable, because they do not make predictions by themselves,
but provide general frameworks for more specific theories, which do
make predictions’ (quoted in Horgan 2015). By this yardstick,
Hamilton’s Rule can be said to be doing rather well. For example, while
the mathematical details of Axelrod and Hamilton’s game theoretical
‘tit-
for-
tat’-
models (Axelrod and Hamilton 1981) and Taylor and
Frank’s kin selection differential equations (Taylor and Frank 1996)
are quite different, they can both be can be translated into the general
framework and shown to satisfy the rb > c inequality.
The price of this generality is that in such comparisons r, b, and c,
are no longer meaningful separate entities. Rather, what matters is c
and the compound entity rb. Should this be called Hamilton’s Rule?
Would it not be more accurate to rename rb as a single, rather than a

compound entity? One might say that still calling this Hamilton’s
Rule, despite the intuitive notions of cost and benefit no longer resid-
ing in b and c, is an artificial attempt to keep an old notation that is no
longer relevant.Whatever one calls it, the general version of Hamilton’s
Rule does make it possible to see biological phenomena as disparate
as limited dispersal, shared habitat preferences, kin recognition, green-
beards, and horizontal gene transfer all as mechanisms that can gener-
ate a positive genetic correlation between actor and recipient of a
given social behaviour. By the same token, punishment, reciprocity,
linkage, and pleiotropy are all mechanisms that link behaviours that
are costly in the short-term but that have a long-term direct fitness
benefit.
The value one assigns to grouping such different biological phe-
nomena may differ. If one is primarily interested in specific adapta-
tions at the organismal level, they may be so different as to make their
grouping uninteresting. Under the gene’s-eye view, the central ques-
tion is typically a version of ‘under these circumstances, will gene G
be selected for or against?’ By this view, the above unification is in no
way a trivial achievement.
4.3 The gene’s-eye view and inclusive fitness:

equivalence or historical accident?
Both Williams and Dawkins saw a great deal of value in the concept
of inclusive fitness and both repeatedly stressed its equivalence with
the gene’s-eye view. Williams even came tantalizingly close to dis
covering kin selection in 1957 in a paper with his wife Doris (Williams
and Williams 1957). In Adaptation and Natural Selection, published only
a few years after Hamilton’s key papers, Williams wrote:
Genic selection should be assumed to imply the current conception of
natural selection often termed neo-Darwinian. An organic adaptation
would be a mechanism designed to promote the success of an individual
organism, as measured by the extent to which it contributes genes to

later generations of the population of which it is a member. It has the
individual’s inclusive fitness as its goal. (Williams 1966, pp. 96–97).
Thus, genic selection and organisms acting to maximize their inclu-

sive fitness are two sides of the same coin. This point has also been
made by Dawkins several times. He once defined (with Hamilton’s
approval, as he was careful to point out) inclusive fitness as ‘that prop-
erty of an individual organism which will appear to be maximized
when what is really being maximized is gene survival’ (Dawkins 1978;
see also Dawkins 2015a, p. 318; Table 4.1).
Table 4.1. The equivalence between genic selection
and inclusive fitness
Unit of selection Role Quantity maximized
Gene Replicator Survival

Individual organism Vehicle Inclusive fitness
Hamilton himself often used a gene’s-eye view early in his career.

After his 1963 and 1964 publications on social behaviour, he moved
onto thinking about sex ratios. In his 1967 paper ‘Extraordinary sex
ratios’ in Science, he tackled Fisher’s argument of why the sex ratio in
most species is 1:1 (Hamilton 1967). Fisher’s argument, which has
been described as ‘probably the most celebrated argument in evolu-
tionary biology’ (Edwards 1998), goes as follows. Suppose that one of
the sexes is rarer than the other. Any parent who can adjust the sex of
their offspring towards that of the rarer sex will now produce off-
spring with higher fitness. Genes leading to the production of the
rarer sex will therefore spread, but the selective benefit of these genes
will diminish the closer the population gets to 1:1.
Hamilton demonstrated that Fisher’s argument does not hold
equally for all genes. In the heterogametic sex, males in XY systems
and females in ZW systems, the sex determining chromosome (Y or W)
does not ‘care’ about the homogametic sex. As a consequence, if a
gene that affects the sex ratio of the offspring that a parent produces
is located on the Y or W it can result in deviations from the 1:1 ratio,

what Hamilton called ‘extraordinary’ sex ratios. Hamilton’s point
highlights the potential for conflict among genes over sex ratio.
Genomic conflict is arguably a phenomenon that makes most sense
from the gene’s-eye view, but it was largely a theoretical speculation
at the time Hamilton was writing. By now, the study of genomic con-
flicts is a thriving field, and how the gene’s-eye view helps make sense
of such conflicts is a major theme of Chapter 5.
Hamilton was also very willing to publicly speak up for the gene’s-
eye view. As mentioned earlier, he wrote a very enthusiastic review of
The Selfish Gene for Science (Hamilton 1977a) and in a letter to the
editor forcibly protested Richard Lewontin’s critical review for Nature
of the same book (Lewontin 1977a; Hamilton 1977b). On the other
hand, he seems to have preferred the individual-centred inclusive fit-
ness concept over the gene’s-eye view. Take this passage from his
comprehensive review of altruism in social insects:
A gene is being favored in natural selection if the aggregate of its rep-
licas forms an increasing fraction of the total gene pool. We are going
to be concerned with genes supposed to affect the social behavior of
their bearers, so let us try to make the argument more vivid by attrib-
uting to the genes, temporarily, intelligence and a certain freedom of
choice. Imagine that a gene is considering the problem of increasing
the number of its replicas… (Hamilton 1972)
An argument straight out of the gene’s-eye view playbook! Yet, only a

few paragraphs later he writes: ‘We can now abandon the fanciful
viewpoint of individual genes’ and writes the rest of the paper from
the perspective of the inclusive fitness interests of the individual
organism. It should be emphasized that Hamilton never explicitly
rejected the gene’s-eye view. As far as I can tell, he considered the
gene’s-eye view and inclusive fitness to be fully compatible, two inter-
pretations of the Necker cube (Table 4.1).
Nevertheless, the failure to fully commit to his own conceptual
revolution appear to have frustrated some of his biggest supporters.
Both Richard Dawkins and John Maynard Smith viewed inclusive
fitness a sound concept, but unnecessarily messy and prone to misun-

derstandings. ‘Paradoxically, the logical conclusion to his ideas should
be the eventual abandonment of his central concept of inclusive fit-
ness’, as Dawkins (1978) put it. Both thought that Hamilton intro-
duced the concept to save the individual as the central player in
evolution and so did not follow through on his own logic and embrace
a gene’s- eye view. In The Extended Phenotype, Dawkins wrote:
‘Historically, indeed, I see the concept of inclusive fitness as the instru-
ment of a brilliant last-ditch rescue attempt, an attempt to save the
individual organism as the level at which we think about natural
selection’ (Dawkins 1982a, p. 187). In Brief Candle in the Dark, Dawkins,
in characteristic prose, describes inclusive fitness as a ‘regrettably cum-
bersome bending over backwards to rescue the individual as the focus
of our Darwinian attention instead of the gene’ (Dawkins 2015a,
p. 319). Maynard Smith, in equally characteristic prose, simply called it
‘an absolute swine to calculate’ and expressed his bafflement as to why
Hamilton moved away from his genic explanation of the 1963
American Naturalist paper only to present ‘a very, very, much more dif-
ficult model’ (Maynard Smith 1997).
For the past decade or two, Dawkins has only rarely intervened in
evolutionary debates. One issue that has proved the exception has
been inclusive fitness and group selection. For example, in 2008 he
wrote to the New Scientist to register his displeasure at an article out-
lining E.O. Wilson’s new-found rejection of kin selection in favour of
group selection (Fanelli 2008; Dawkins 2008b). Wilson had been an
early supporter of Hamilton’s work (though inclusive fitness is mis-
defined in Sociobiology, as Grafen 1982 has pointed out). T owards the
end of his career, however, he has come out strongly against it. T he
New Scientist piece largely stemmed from a paper Wilson wrote for
Bioscience, where he used examples from eusocial insects to argue
against inclusive fitness theory (Wilson 2008). T hen, 2 years later,
he teamed up with Tarnita and Nowak to publish the theory-heavy
‘The evolution of eusociality’ (Nowak et al. 2010). At a plenary talk
during the 2016 meeting for The International Society of Behavioural
Ecology in Exeter, UK, Dawkins would say that Nature’s decision to

publish Nowak et al. (2010) had turned the journal into the ‘National
Enquirer of science’.
In 2012, Dawkins also published two short essays going hard against
Wilson’s conversion. One was a review of Wilson’s book length version
of his argument (Wilson 2012), which Dawkins dismissed using the
popular witticism ‘not a book to be tossed lightly aside. It should be
thrown with great force’ (Dawkins 2012a). T he other was a more positive
commentary on Steven Pinker’s ‘The false allure of group selection’
(Pinker 2012), where he reiterated his call for talking about replicators and
vehicles instead of individual and group selection (Dawkins 2012b).
Group selection thus still appears to be the button on the back of
Dawkins’s head that can be most effectively pushed. Dawkins and the
modern-day critics of inclusive fitness may, however, have more in
common than they would probably like to admit. Take the following
two quotes:
What matters is gene selection. All we need ask of a purportedly adap-
tive trait is, ‘What makes a gene for that trait increase in frequency?
(Author 1)
We may rely on a straightforward genetic approach: Consider m utations
that modify behavior. Under which conditions are these mutations
favored (or disfavored) by natural selection? The target of selection is
not the individual, but the allele or the genomic ensemble that affects
behavior. (Author 2)
Both are arguing against thinking in terms of individuals and/or

groups, and for focusing on gene level selection. The first is from
Dawkins (2008b) critiquing Wilson’s group selectionism and the sec-
ond from Allen et al. (2013) where Nowak and Wilson were joined by
Benjamin Allen to describe the limitations of inclusive fitness.
The complaint that inclusive fitness is unnecessarily complicated,
prone to misunderstanding, and that one should just focus on whether
an allele with a given effect on social behaviour will invade the
population is thus shared by unlikely bedfellows. When speaking at
the Oxford Union, a debating society, in February 2014, Dawkins
conceded that Nowak and colleagues are correct that inclusive fitness
is often very difficult to calculate in practice (Dawkins 2014). At the
same time, he insisted that inclusive fitness follows deductively from
population genetics and that the way to prove it is not through
experiment, but logically, just as one would not prove Pythagoras’s
Theorem by measuring angles with a ruler in nature. Dawkins con-
cludes his reasoning by saying that he would prefer to ‘forget about
inclusive fitness and go straight to the level of the gene’. Nowak and
colleagues are in this way joining a longstanding critique of inclusive
fitness.
Part of the problem could be that there appears to be some confu-
sion among the authors of Nowak et al. (2010) about whether or not
their model is actually a critique of the gene’s-eye view. T he main
paper is largely a group-selection flavoured verbal model, whereas the
meaty appendix relies on a gene- centric mathematical approach.
Following the paper’s publication, the authors have also given some-
what contradictory statements. For example, in an interview with The
Guardian, a British broadsheet, E.O. Wilson said of selfish gene think-
ing: ‘I have abandoned it and I think most serious scientists working
on it have abandoned it. Some defenders may be out there, but they
have been relatively or completely silenced since our major paper
[Nowak et al. 2010] came out’ (Johnston 2014). At the same time,
Nowak, Tarnita, and Wilson write in the 2010 paper: ‘A “gene-
centered” approach for the evolution of eusociality makes inclusive
fitness theory unnecessary’ (Nowak et al. 2010). A similar point is
reiterated in a statement signed by all three authors on website of
Harvard’s Program for Evolutionary Dynamics, where Nowak is the
director: ‘our model for the evolution of eusociality is not a group
selection model; instead it describes selection operating at the level of
genes’ (Nowak et al. 2011). T hus, critics of Hamilton’s work like,
at least some of the time, to frame their argument in terms of gene
selectionism. T his kind of rhetoric is also evident in Nowak’s contri-
bution on inclusive fitness to the edited volume This Idea Must Die
(Nowak 2015). Demonstrating the difficulty (some would say futility)
in trying to sort opinions under clear labels, Nowak himself resists the
term ‘gene’s-eye view’ preferring ‘population genetics’ or ‘evolution-
ary dynamics’ (M.A. Nowak, personal communication).
4.3.1 Formal connections between the gene’s-eye view

and Hamilton’s Rule
What, then, are the actual formal connections between the gene’s-eye
view and Hamilton’s Rule? Andy Gardner, one of the most enthusias-
tic defenders of Hamilton’s work, has questioned the commonly held
view that the two are intimately linked. In the fun ‘Kin selection
under blending inheritance’, Gardner addresses the suggestion that
the reason why Darwin failed to develop a proper theory of kin selec-
tion was that he lacked a functional theory of inheritance
(Gardner 2011). He points out that because the current version of
Hamilton’s rule relies on the Price equation, which can handle any
form of inheritance, it does not require discrete Mendelian inherit-
ance. A breeding value does not necessarily have to be calculated from
the weighted sum of allelic values.
By re-deriving the general version of Hamilton’s Rule without
assuming any particular inheritance, Gardner shows that blending
inheritance complicates the computation of relatedness coefficients
but does not in any way make their calculation impossible. Crucially,
predictions remain the same regardless whether inheritance is
Mendelian or blending. Based on this, Gardner argues that the indi-
vidual organism is the unit of selection and adaptation, and that the
gene’s-eye view will only play this role in limited cases, such as
those involving genomic conflicts. According to this argument, the
strong connection between the gene’s-eye and Hamilton’s Rule
stems less from formal links and more from their historical
association.
There are other reasons, however, to view the two as being con-
nected in a formal, though subtle, way. T
o see why, let’s revisit the der
ivation of Hamilton’s Rule outlined in Box 4.1 and explore how the
gene’s-eye view fits in. The derivation shows why the general version
of Hamilton’s Rule works best under a genic view of the environ
ment. Focusing on Cov(wi,pi) allows the natural selection part of evo-
lutionary change to be captured, but only in a constant environment.
Making such an assumption requires us to think, as Fisher did, of the
environment of a given allele to include not just the external envir
onment, but also the rest of the genome (Fisher 1918). From the per-
spective of an individual organism, conceptualizing any changes in the
genomic context (other genes in the genome and in the gene pool)
that an allele may find itself in as environmental makes little sense.
From the gene’s-eye view it is straightforward. The only way that
Cov(wi,pi) can be taken to capture natural selection in a constant envir
onment is if this gene’s-eye view of the environment is adopted. T he
connection between inclusive fitness theory and the gene’s-eye view
may appear to be a subtle point in the derivation of the general ver-
sion of Hamilton’s Rule, but it demonstrates that the intimate rela-
tionship is not just a historical accident.
Examining the general version of Hamilton’s Rule also opens an
interesting door to some potential tensions with the gene’s-eye view.
Recall that a key step in Queller’s derivation of the general version of
Hamilton’s Rule is that the transmission term, E ( w i Dpi ), of the Price
equation is assumed to be 0. T his means that genetic drift, among
other things, is ignored, which is usually acceptable if the primary
concern is adaptation. From a gene’s-eye view, a more important con-
sequence is that it forces us to ignore within-organism selection due
to, for example, meiotic drive or other forms of genomic conflict. T his
is a rather high price to pay. That all genes work together for the same
purpose is a crucial assumption of many inclusive fitness models. T he
gene’s-eye view, however, stresses that such unity of purpose cannot
just be taken for granted. It is there and it must be explained.
To see whether this potential tension actually manifests, I next
examine the tradition in evolutionary biology that has sought to use
inclusive fitness as the answer to the question of what is it that organ-
isms should appear designed to be trying to maximize. I therefore
turn to this tradition’s most ambitious version, Alan Grafen’s Formal

Darwinism Project.
4.4 Maximization of inclusive fitness and the

Formal Darwinism Project
The Formal Darwinism Project takes as its starting point what it con-
siders to be Darwin’s central insight: that evolution by natural selec-
tion provides a way by which a purely mechanistic process (inheritance
and reproduction) can give rise to the appearance of design in the
living world (see also Dennett 1995 and Haig 2020). Its goal is to for-
malize this insight. T
he chief architect of this unification effort is Alan
Grafen, who received his undergraduate degree in experimental
psychology and a master’s degree in economics before doing his doc-
torate in evolutionary biology under Dawkins’s supervision. T ogether
with Andy Gardner, he is probably the best representative of the con-
temporary neo-Paleyan tradition in British biology introduced in
Chapter 1.
Grafen seeks to construct a mathematical bridge between the
dynamic models of population genetics that capture changes in gene
frequencies and the optimality models that describe fitness maximiza-
tion. By doing so, he wants to mathematically justify the ‘individual-
as-maximizing-agent analogy’, which he argues is an analogy taken
for granted by many empirical biologists, especially behavioural
ecologists, but is one that lacks formal grounding. Grafen’s bridge-
building attempt began with Grafen (1999) and now spans several
papers, many abstract and technical even for biologists with a serious
theoretical bent. Grafen (2007) and Grafen (2008) offer non-
mathematical overviews and the 2014 special issue of Biology and
Philosophy provides an introduction to the many conceptual issues of
the project (see the opening paper by the editors Okasha and
Paternotte 2014 and Grafen’s outline and response to the eleven com-
menting papers; Grafen 2014a; 2014b).
The Formal Darwinism Project is the most comprehensive expres-

sion of a broader tradition that views inclusive fitness as the answer to
the design objective of natural selection, i.e. what organisms should
appear to maximize. If both defenders and critics agree that there are
some mathematical shortcomings to inclusive fitness, they disagree
over how comfortable one can be with them. Key to predicting
whether someone can live with these limitations seems to be whether
they share the neo- Paleyan assumption underlying the Formal
Darwinism Project. Authors like Allen and Nowak firmly reject this
notion and see no need for any kind of design principle (Allen et al.
2013; Allen and Nowak 2016).
Those who do take adaptation to be a special problem are more
likely to be comfortable with the assumptions required to make
models of maximizing inclusive fitness work (West and Gardner 2013;
Marshall 2015; Levin and Grafen 2019). For example, such models
often assume that selection is weak and that the fitness effects of social
behaviour are additive. Advocates of inclusive fitness concede these
points and instead emphasize another aspect of the general version of
Hamilton’s Rule. Just as the point of Hamilton’s Rule is to provide an
organizing framework rather than exact testable predictions for every
conceivable biological scenario, inclusive fitness is not just another
mathematical approach. Instead, it explains what organisms should
appear designed to act as if to maximize (West and Gardner 2013;
Levin and Grafen 2019; see also Lehmann and Rousset 2020;
Paternotte 2020). From this, it also follows that cooperation and con-
flict can be modelled as situations where the inclusive fitness interests
align or diverge, which is why it can be such a powerful and popular
tool in social evolution.
4.4.1 Genes versus individuals in the Formal

Darwinism Project
There has always been a connection between the gene’s-eye view
and the Formal Darwinism Project. In 2011, when Grafen teamed up
with the mathematician Charles Batty, like Grafen a fellow at St John’s

College, Oxford, to advertise for two postdoc positions in mathemat-
ics to work on the Formal Darwinism Project, the project was
advertised with the title ‘The deep mathematical theory of selfish
genes’. As with the gene’s-eye view’s general relationship with inclu-
sive fitness, however, there is also some tension. Recall that the
existence of such tension is perhaps not surprising. Dawkins warned
of the ‘theoretical dangers’ associated with thinking in terms of indi-
viduals maximizing their fitness (Dawkins 1982a, p. 91) and he further
wrote of Hamilton that:
instead of following his ideas through to their logical conclusion and

sweeping the individual organism from its pedestal as notional agent of
maximization, he exerted his genius in devising a means of rescuing
the individual. He could have persisted in saying: gene survival is what
matters; let us examine what a gene would have to do in order to
propagate copies of itself. Instead he, in effect, said: gene survival is
what matters; what is the minimum change we have to make to our old
view of what individuals must do, in order that we may cling on to our
idea of the individual as the unit of action? (Dawkins 1982a, p. 196)
Grafen long emphasized that ‘the organismal approach is not in con-

flict with the “gene selectionism” of Dawkins’ (Grafen 1984). In the
early papers of the Formal Darwinism Project, Grafen explicitly
framed the aims of the Formal Darwinism Project in terms of formal-
izing insights from Dawkins and Williams (Grafen 1999, 2002, 2007).
In more recent papers, the gene’s-eye view has taken a back seat. For
example, Levin and Grafen (2019) write that ‘the selfish gene approach
can be useful for certain gene level questions, such as intragenomic
conflict’. If one grants the premise of the Formal Darwinism Project—
that Darwin unified mechanism and purpose and that the appearance
of design is at the heart of that—why should the effort to formalize
this unification privilege an individual over a gene- centric
perspective?
One way to think about it is that only organisms can be said to
manifest complex adaptations. Gardner (2014b) makes this point by
appealing to Paley’s criteria for complex design: contrivance and

relation (see Chapter 1). Genes, he argues, satisfy one of the two cri-
teria, organisms satisfy both. Contrivance captures how an entity
appears designed for a specific purpose. Genes can satisfy this require-
ment, whether it is to produce a certain protein or to regulate the
expression of other genes. Even if genes can have many functions,
however, they do not come near the repertoire of traits and functions
that a whole organism can manifest. They therefore fail to meet the
‘relation of parts’ requirement.
How parts of the organisms work together is also key to another
potential tension point between genic and organismal approaches to
adaptation. How should conflict among genes be handled? Hamilton
captured the issue rather poetically:
Seemingly inescapable conflict within diploid organisms came to me as

both a new agonizing challenge and at the same time as a release from
a personal problem I had had all my life (…) Given my realization of an
eternal disquiet within, couldn’t I feel better about my own inability to
be consistent in what I was doing, about indecision in matters ranging
from daily trivialities up to the very nature of right and wrong? (…) As
I write these words, even as to be able to write them, I am pretending
to a unity that, deep inside myself, I now know does not exist. I am
fundamentally mixed, male with female, parent with offspring, warring
segments of chromosomes… (Hamilton 1996, pp. 134–134).
There is an argument that for an entity to be able to evolve adapta-

tion, all parts of that entity must work towards the same goal and there
can be little to no selection within that entity (Gardner and
Grafen 2009; West and Gardner 2013; Gardner 2014a, 2014b;
Grafen 2014a). T hat is, the parts must demonstrate a unity of purpose.
At the gene level, this means no genomic conflict. Recall that the
derivation of the general form of Hamilton’s Rule comes with an
assumption of perfect genetic transmission, i.e. fair meiosis such that
E ( w i Dpi ) equals 0, and so no role for segregation distorters and other
kinds of selfish genetic elements (Box 4.1). Grafen’s Formal Darwinism
models make the same assumption.
Selfish genetic elements have the potential to undermine the unity

of purpose required for this assumption. Their existence raises the
question whether it is appropriate to treat the individual organism as
the sole fitness maximizer (Okasha 2018, p. 29). As Dawkins put it:
‘There is a sense in which a “vehicle” is worthy of the name in inverse
proportion to the number of outlaw replicators that it contains’
(Dawkins 1982a, p. 134). Here, it is worth emphasizing that it is not
that the Formal Darwinism Project has nothing to say about genomic
conflicts. Whereas Grafen (2014b) admits that he has often tended to
downplay their significance, genomic conflicts can be studied using
its methods. Because it links replicator dynamics to maximization
principles, its models can be applied to different part of the genome
(say maternally inherited mitochondrial genes versus biparentally
inherited autosomal genes), which allows an account of genomic
conflicts to be developed (see Gardner and Welch 2011 and Gardner
and Úbeda 2017). Rather, the implicit assumption is that if the goal
is to understand organismal adaptations, such conflicts can be
ignored. Whether such an assumption is reasonable is ultimately an
empirical question.
Inclusive fitness theorists have generally relied on the so-called
‘phenotypic gambit’. T his is the assumption that selection on a trait
will not be constrained by its genetic architecture (Grafen 1984).
While recognizing that this assumption will often be violated, such as
in the case of heterozygote advantage, it is suggested that it is justified
because of its track record making empirically testable predictions
(Grafen 2014a; Levin and Grafen 2019). Theoretically, the assumption
is handled by assuming that the trait in question is captured by a hap-
loid population genetic model with a separate allele for each possible
phenotype. When such genic consensus cannot be achieved, the
phenotypic gambit fails. T
his may happen, for example, when a single
trait is affected by genes inherited in different ways, say by both
maternally inherited mitochondrial genes and biparentally inherited
autosomal genes. Such transmission asymmetries are a common
source of genomic conflict (Cosmides and Tooby 1981; Burt and
Trivers 2006; Ågren and Clark 2018) and may result in the fragmenta-

tion of individual fitness maximization.
Haig has argued that the ubiquity of genomic conflict leaves biolo
gists interested in adaptation with two possible options (Haig 2014).
The first is the one offered by the Formal Darwinism Project, which
suggests that such conflicts can typically be ignored. From a gene’s-
eye view this goes too far. Under the second solution, the one
advocated by Haig, the individual organism is viewed as an

‘adaptive compromise’, rather than a unified fitness maximizer

(Haig 2006b, 2014). As Maynard Smith argued, the gene’s-eye view
forces us to think about what individual organisms are to begin with
and why and how it achieves its unity of purpose (Maynard
Smith 1982a, 1985). As he put it: ‘How did it come about that most
genes, most of the time, play fair, so that a gene’s success depends only
on the success of the individual that carries it?’ (Maynard Smith 1985)
Maynard Smith would return to this question when he published
The Major Transitions in Evolution together with Eörs Szathmáry
(Maynard Smith and Szathmáry 1995). As outlined in Chapter 2, they
put forward the idea that life’s hierarchy is a consequence of a series
of events where new entities evolved by the coming-together of
entities that were previously surviving and reproducing on their own.
A crucial step in these transitions is the suppression of conflict at
lower levels. T
his process is never complete, and the unity of the indi-
vidual is therefore constantly threatened from within. Genomic con-
flicts are not just a curiosity with little evolutionary significance but
exactly what should be expected.
The gene’s-eye view and the Formal Darwinism Project share the
neo-Paleyan commitment to adaptation being the main question that
evolutionary theories should aim to explain. One difference is which
of Lloyd’s four questions that they are primarily interested in.Whereas
the Formal Darwinism Project is concerned with a combination of
the interactor and manifestor of adaptation questions, the gene’s-eye
view is focused on the beneficiary question. The major transitions
framework can provide a productive bridge between the individual-
as-maximizing-agent analogy and the gene’s-eye view, as advocated

by Bourke (Bourke 2011, 2014). T he gene’s-eye view, especially when
paired with a major transitions framework, drums home that this
analogy is conditional on the unity of purpose of genes.
4.5 Recent reconciliations between the

gene’s-eye view and inclusive fitness
This brief historical sketch demonstrates the intimate relationship

between the gene’s-eye view and inclusive fitness. The ties between
the two perspectives are deep and when frustrations have arisen it has
usually been from the side of the gene’s-eye view, as exemplified by
the comments from Maynard Smith and Dawkins. My impression is
that most biologists are happy to keep both perspectives around, using
either depending on the goal of the moment. As Krebs and Davies put
it in one of their classic textbooks:
‘the field biologist sees individuals dying, surviving and reproducing;

but the evolutionary consequence is that the frequencies of
genes change. Therefore the field biologists tend to think in terms
of individual selection whilst the theorists thinks in terms of selfish
genes.’ (Krebs and Davies 1993, p. 375; original emphasis)
This pluralistic pragmatic approach is very sensible. Different prob-

lems will often demand different tools. That being said, exploring
how the two perspectives are related is interesting and worthwhile in
of itself. T
here are numerous papers on inclusive fitness published
every year, by theorists and empiricists, and by critics and supporters.
Here, I am less interested in what this new work can tell about inclu-
sive fitness theory than what light it can shine on the gene’s-eye view.
Two recent papers on inclusive fitness theory explicitly frame their
argument in terms of the gene’s-eye view (Akçay and Van Cleve 2016
and Fromhage and Jennions 2019) and I will end this chapter by dis-
cussing them.
Both papers touch an especially contentious point in the current

debate over inclusive fitness, which is whether inclusive fitness is a
causal property that belongs to the individual organism. Hamilton was
clear that this was his definition, and supporters of inclusive fitness
have made much of the fact that inclusive fitness is a unique definition
of fitness in that it is the only one that is both a target of selection and
under the organism’s control. Causal control is important because
they argue that an entity can only appear designed for something that
it has full control over, which makes inclusive fitness special even rela-
tive to closely related concepts, such as neighbour modulated fitness
(Gardner et al. 2011;West and Gardner 2013; Marshall 2015; Levin and
Grafen 2019). Again, critics deny this point (Allen and Nowak 2016).
Akçay and Van Cleve (2016) and Fromhage and Jennions (2019)
both touch on the causal property issue but suggest rather different
solutions and, in their own ways, challenge Hamilton’s original defin
ition of inclusive fitness. Akçay and Van Cleve reject Hamilton’s argu-
ment that inclusive fitness is an extension of classical fitness and
suggest that it does not actually belong to the individual but that it is
a property of the genetic lineage, that is all copies stemming from an
original mutation. Fromhage and Jennions, in turn, suggest re-defining
inclusive fitness to align with what they call the folk definition of
inclusive fitness. Such a definition, they argue, would allow inclusive
fitness to be properly be reconciled with a gene’s-eye view.
4.5.1 The genetic lineage view of inclusive fitness

The central argument of Akçay and Van Cleve (2016) is that many of
the potential pitfalls of inclusive fitness theory can be avoided if inclu-
sive fitness is re-conceived as a property of the genetic lineage rather
than of the individual organism. They base their conclusion on a
pretty straightforward population genetic argument, where they con-
sider a haploid population and ask when a rare mutation can invade
the population. T his kind of fitness, called invasion fitness, is in its
most basic form the geometric mean growth rate of a rare mutation
in a population. While this quantity, which can be denoted g, captures

all that is needed to predict the long-term fate of the mutation over
evolutionary time (it will invade as long as g > 1), it does not neces-
sarily lend itself to much of a biological interpretation.
For a fitness definition like this to have meaning for empirically
minded biologists, whether in the lab or in the field, it needs to be
translated into more concrete terms. In practice, this has often meant
number of surviving offspring per individual per lifetime. Denoted w,
personal fitness is typically calculated by theorists as the average num-
ber of surviving offspring of a given genotype. Because any potential
stochastic effects stemming from biotic or abiotic factors can be
accounted for by averaging in a certain way, the remaining variation
in w will come from the focal individual’s social partners. By explicitly
considering these interactions, Akçay and Van Cleve point out that
individual and inclusive fitness can be linked so that the fitness of an
individual carrying the rare mutation, wm, can be expressed as a linear
function of how common the rare mutation is among the social part-
ners of the focal individual carrying the rare mutation, pn:
w m = 1 - c + bpn + e
Where 1 is the baseline fitness of the non-mutant genotype; c is the
direct fitness effect, the effect of the mutation on the fitness of the
individual that carries it, and b is the indirect fitness effect, how other
individuals affect the fitness of the individual that carries the muta-
tion. e is an error term. The next step is to determine the expected
fitness of the mutant across all social partners, which is achieved by
considering all possible frequencies of the rare mutation among social
partners. This expected term E[wm] will be the inclusive fitness, wIF
such that:
E[w m ] = w IF = 1 - c + br .
where r here is defined as the expectation that a random social partner
will be of the same mutant lineage. If fitness effects are additive, this
definition is the same as Hamilton’s original definition of inclusive
fitness. In this model, the value of b and c do not depend on the
frequency of the rare mutation, and the mutant’s fitness can be cap-
tured by a linear model. T his fact allows wIF to be linked to invasion
fitness so that the rate at which the mutation is spreading is the inclu-
sive fitness of that mutation lineage. In other words:
g = w IF = 1 - c + br
Since a rare mutation will invade when g > 1, the above expression
can be rearranged to that say that the rare mutation will spread when
the inequality rb > c is satisfied. Akçay and Van Cleve thus recover
Hamilton’s Rule while connecting the simple theoretical concept of
invasion fitness, g, to a more practical concept of individual fitness, w.
Akçay and Van Cleve’s definition of the inclusive fitness of a gene
comes with two key implications. The first is that it no longer makes
sense to think of inclusive fitness as a generalization of classical fitness,
as Hamilton originally did. Inclusive fitness is simply the fitness of a
genetic lineage averaged across all possible states the lineage may find
itself in, including genetic backgrounds, population structures, and
biotic and abiotic environments. The second implication is that it
transfers inclusive fitness from the individual organism to the genetic
lineage. As discussed, the fact that inclusive fitness is under the full
control of the individual organism is often cited as a key advantage of
inclusive fitness theory. Relinquishing this may therefore be a big pill
to swallow. Whereas Dawkins and Williams never used these exact
terms, this move from organism to genetic lineage should be easier to
accept for proponents of the gene’s-eye view.
4.5.2 The folk definition of inclusive fitness and the

parliament of genes
The goal of Fromhage and Jennions (2019) was to ‘tidy up’ the gene’s-
eye view by resolving its tension with inclusive fitness models centred
on individuals. Such tidying is necessary, they argue, because there is a
danger in focusing exclusively on genes. Despite the impressive preci-
sion with which theoretical population geneticists can construct
mathematical models describing the conditions under which an allele

with certain hypothetical properties is favoured by natural selection,
the fact remains that many evolutionary biologists are usually more
interested in the question of whether a given phenotype is adaptive or
not. As helpful as the gene’s-eye view can be for working out the logic
of natural selection, it will always be impotent unless it can be prop-
erly connected to traits of actual organisms (Hammerstein 1996).
To get around this, Fromhage and Jennions suggest that the current
definition of inclusive fitness should be discarded. In its place, they
want the field to adopt a more intuitive version that they dub ‘folk
inclusive fitness’, a version long repudiated by inclusive fitness theor
ists (e.g. Grafen 1982). This is quite a radical step (see Queller 2019 for
a primer), especially as they argue that their definition can handle two
of the main criticisms levelled at inclusive fitness: non-additive fitness
interactions and mutations of various effect sizes.
Their new definition of inclusive fitness is a product of changing
the way its calculated. Recall from earlier that to properly calculate an
individual’s inclusive fitness it has been considered crucial to deduct
the part of the direct fitness that is due to actions of the social envir
onment. Fromhage and Jennions suggest that this subtraction step can
be dropped, leaving what they call a ‘folk definition’ of inclusive fit-
ness. The flipside of this definition, they argue, is that it makes inclu-
sive fitness a quantity that when maximized also results in what is best
for the ‘majority interest’ of the genome, thus linking a genic with an
individual centred perspective.
Fromhage and Jennions’ account seeks to combine Dawkins’s
vehicle concept with Egbert Leigh’s ‘parliament of genes’ (Leigh 1971).
Leigh introduced the idea of a parliament of genes in the context of
the evolution of fair meiosis, i.e. that each allele in a diploid organism
has a 50% chance of being transmitted. Discussing the potential select
ive advantage of a meiotic driver, a gene promoting its own transmis-
sion beyond 50%, he wrote: ‘It is as if we had to do with a parliament
of genes: each acts in its own self-interest, but if its acts hurt others,
they will combine together to suppress it’ (Leigh 1971, p. 249). That is,
even if meiotic drivers, or any other genes that can promote their own
transmission at the expense of other genes, are initially favoured, their
spread will be counteracted by selection at other unlinked loci, and
because there will be more such loci, they will serve the ‘majority
interest’ (see also Scott and West 2019). According to Fromhage and
Jennions, the ‘majority interest’ of the genome is best served by pro-
ducing organisms with high ‘vehicle quality’, as measured by the abil-
ity to produce copies of the organism’s genes. More specifically, high
vehicle quality is measured by counting copies of a hypothetical gene
with idealized properties, a ‘reference gene’, which represents the
genome’s majority interest.
The reference gene (as is often the case with the gene’s-eye view,
the ‘gene’ in question is actually an allele) has four key properties:
1. It is carried by the focal organism.

2. It is present at a low frequency in the population.
3. Its transmission is Mendelian.
4. It is never or rarely expressed.
These four properties serve two main functions: allowing the number
of reference genes to be counted (properties 1 and 2) and to guarantee
that a reference gene is a good stand-in for the genome’s majority
interest (properties 3 and 4).
Estimating vehicle quality by the number of reference gene copies
that a focal individual is causally responsible for means that it can be
quantified as follows. Under sexual reproduction, the probability of a
reference gene being transmitted from parent to offspring is given by
s. Assuming outbreeding, s = 0.5. Pedigree relatedness is given by r,
and the number of propagated reference gene copies is captured by
the expression s × Σ(r × Δr), where Δr is the additional offspring pro-
duced by relatives with relatedness r, as caused by the focal
organism.
This way of doing the sums counts all the offspring of the focal
individual, and thus it does not include the ‘stripping’ part of
Hamilton’s original definition. This ‘folk definition’ of inclusive fit-

ness is therefore maximized when the expected value of Σ(r × Δr) is
maximized. Because this happens when the majority interest of the
genome is satisfied, Fromhage and Jennions argue that this offers a
way to handle genomic conflicts.
Fromhage and Jennions’ solution to the tension between the gene’s-
eye view and inclusive fitness is quite different to the one offered by
Akçay and Van Cleve. Fromhage and Jennions retain the organism as
a central unit, but they do so while simultaneously trying to take con-
flicts between genes seriously in a way that the Formal Darwinism
Project usually does not. Akçay and Van Cleve moved inclusive fitness
from the organism down to the gene, which can be more readily
accepted by those with a gene’s-eye view and arguably comes close
to Williams’ and Dawkins’s thinking. At the same time, both Williams
and Dawkins did think the design-like features of organisms were
something special and if our explanations completely leave them
out in favour of focusing on one gene at a time something is
missing.
4.6 Summary
• W.D. Hamilton provided one of earliest clear articulations of the

gene’s-eye view and there is a long-standing, intimate, relationship
between the gene’s-eye view and the concepts of inclusive fitness,
kin selection, and Hamilton’s Rule.
• For pragmatic purposes, the gene’s-eye view and inclusive fitness
can often be thought of as equivalent, two sides of a Necker cube:
genes are replicators that try to maximize their survival and organ-
isms are vehicles maximizing their inclusive fitness. At the same
time, Dawkins and Maynard Smith, both admirers of Hamilton,
complained that he did not follow through on his own conceptual
revolution in fully shifting from an organismal to a genic
perspective.
• Inclusive fitness and Hamilton’s Rule have recently come under

much scrutiny. Strikingly, and somewhat ironically, today’s critics of
Hamilton’s work often rely on the gene’s-eye view’s rhetoric and
use arguments similar to those first articulated by Dawkins and
Maynard Smith.
• The Formal Darwinism Project seeks to formally justify that indi-
vidual organisms should strive to maximize their inclusive fitness by
unifying population genetic and optimization models.
Mathematically rather abstract, it is based on an assumption of
genomic unity of purpose that highlights some interesting potential
tension with the gene’s-eye view.
• Despite traditionally thought of as equivalent, there is interesting
contemporary work on the relationship between the gene’s-eye
view and inclusive fitness.
5
Empirical Implications
5.1 Introduction
W hen the Manhattan Project physicist Leo Szilard switched to

biology after the end of the war, he found that this career
change ruined his bath-time. As a physicist, he was accustomed to
starting his day in the bath, while thinking through theoretical prob-
lems in his head (Barry 2005, p. 24). In his new life as a biologist, this
did not work; he had to repeatedly get up to look up a fact, ruining
any attempts of Archimedes-style ruminations.
Biology by its nature is messy, a science of exceptions. In many
corners of biology, the dominant view of science is one where facts
come first and then, in light of those, new theories emerge. In
evolutionary biology at least, that is far from always the case and the-
ory often leads the way. The early success of the gene’s-eye view
stemmed from helping make sense of the field’s old problems,
especially those related to social behaviour. It also had more radical
implications.
Nowhere are these spelled out more clearly than in The Extended
Phenotype (Dawkins 1982a). Every writer has one piece that they
consider their best. Something about which they say: ‘if you read only
one thing of mine, read this!’. For Dawkins, that is The Extended
Phenotype. It was his second book and it is the only book of his that is
aimed at professional biologists, rather than the general public. It is
centred upon the goal of ‘[freeing] the selfish gene from the individual
DOI: 10.1093/oso/9780198862260.003.0006
organism which has been its conceptual prison’ (Dawkins 1982a, p. vi).

The Extended Phenotype remains the most exhaustive articulation and
defence of the gene’s-eye view. The radical nature of its argument is
well illustrated by the afterword by Daniel Dennett that was added to
the 1999 paperback edition:
Is The Extended Phenotype science or philosophy? It is both; it is

science, certainly, but it is also what philosophy should be, and only
intermittently is: a scrupulously reasoned argument that opens our
eyes to a new perspective, clarifying what had been murky and ill-
understood, and giving us a new way of thinking about topics we
thought we already understood (…) [Dawkins] shows how our
traditional way of thinking about organisms should be replaced

by a richer version in which the boundary between organism and
environment first dissolves and then gets partially rebuilt on a deeper
foundation. (Dennett 1999)
This chapter is dedicated to three empirical phenomena whose study

grew out of the gene’s-eye and constitute the core of this new deeper
foundation: extended phenotypes, greenbeard genes, and selfish
genetic elements.
Extended phenotypes are the effects of a gene that occur beyond
the physical body in which the gene resides. Paradigmatic examples
include beaver dams, brood parasitism by cuckoo chicks, and parasite
manipulation of host behaviours. Greenbeard genes are genes that can
recognize copies of themselves in other individuals and then cause
their carrier to act nepotistically toward such individuals. Greenbeards
make clear that, from a gene’s-eye view, for a costly social behaviour
to evolve it is the relatedness at the particular locus that underlies the
social behaviour that matters, not the genome- wide relatedness.
Greenbeards were initially thought to be a fun theoretical idea unlikely
to exist in nature, but several examples have been identified, including
in yeast, slime molds, and ants.
Selfish genetic elements are stretches of DNA that can promote
their own transmission at the expense of other genes in the genome
E m pi r ica l i m plicat ions 153
while having either no effect or a negative effect on organismal fitness.

The first description of selfish genetic elements predates the origin of
the gene’s-eye view, but those examples were usually considered to be
genetic oddities with few implications for evolutionary theory.
Although selfish genetic elements played only a minor role in the
early articulations of the gene’s-eye view, the gene-centred perspective
brought them to the forefront of evolutionary biology. Reciprocally,
selfish genetic elements have often been considered the best evidence
for the power of the gene’s-eye view.
This chapter will be slightly different than the others. Rather than
navigating the intricacies of conceptual debates, I will review empirical
examples that all bolster the gene’s-eye view’s effort to undermine the
centrality of the individual organism in evolutionary explanations. As
Dawkins noted soon after the publication of The Selfish Gene: ‘All
these ideas, even if they appear far-fetched in practice, are perfectly
respectable in theory, and you would never think of them if you based
your ideas on individual fitness rather than on gene replication’
(Dawkins 1978). Selfish genetic elements are also my own area of
research and I will pay particular attention to their biology. I will end
the chapter by discussing how the historical association between the
gene’s-eye view and these empirical examples holds up today,
especially when compared to other proposed frameworks.
5.2 Extended phenotypes
Dawkins introduced the term ‘extended phenotype’ during a talk at

the 15th International Ethological Conference in Bielefeld, Germany
(later published as Dawkins 1978). In The Extended Phenotype, he
summarized the central claim of the concept as: ‘An animal’s behav-
iour tends to maximize the survival of the genes ‘for’ that behaviour,
whether or not those genes happen to be in the body of the particular
animal performing it’ (Dawkins 1982a, p. 233). T
ogether with group
selection, the concept of extended phenotypes has been a rare topic
that has led Dawkins to publicly comment on current debates in

evolutionary biology. Whereas the former has been a reliable trigger
of irritated interventions, work on extended phenotypes has elicited
more enthusiastic ones. In the foreword of a 2012 edited volume on
the topic (Hughes et al. 2012), Dawkins names parasites manipulating
the behaviour of their hosts as his ‘personal epitome of Darwinian
adaptation, the ne plus ultra of natural selection in all its merciless
glory’ (Dawkins 2012c). And in an essay for a special issue of Biology
and Philosophy commemorating the 20th anniversary of The Extended
Phenotype, Dawkins dreams of opening an ‘Extended Phenotypic
Institute’. In the dream, the institute is made up of three departments:
the Zoological Artefact Museum, the laboratory of Parasite Extended
Genetics, and the Centre for Action at a Distance (Dawkins 2004b).
In his autobiography he nominates the entomologist and evolution-
ary biologist David Hughes to be its inaugural director (Dawkins 2015a,
p. 337).
At the same time, Dawkins also admits of being a little disappointed
that empirical research on extended phenotypes has not made more
progress. He notes that whereas the gene’s-eye view is now common
knowledge among professional evolutionary biologists, and some
empirical fields spurred by the concept, such as the study of genomic
conflicts have seen rapid developments, extended phenotypes—the
part of the general theoretical framework of the gene’s-eye view that
he considers wholly his own—is still a minor topic. That might well
be true, but several examples have been described. They can be
organized into three main categories.
5.2.1 Three kinds of extended phenotypes

The wide variety of potential extended phenotypes mean that there are
several ways in which they can be grouped. Here, I have chosen to fol-
low the approach reflected in Dawkins’s imaginary Extended Phenotypic
Institute (see also Hughes 2008, 2012, 2013): animal architecture, action
at a distance, and parasite manipulation of host behaviour.
Animal architecture has long fascinated biologists. In 1974, it was

the name of a book by Karl von Frisch, who in the previous year had
shared the Nobel Prize in Physiology or Medicine with Konrad
Lorenz and Dawkins’s doctoral advisor Nikolaas Tinbergen for their
foundational work on animal behaviour (von Frisch 1974). T he 1999
paperback edition of The Extended Phenotype came with a beaver dam
on the cover and that has often been the textbook example of the
concept.
The beaver dam also serves as a useful starting point for how to
restrict the definition of an extended phenotype. Dawkins (2004b)
describes how lay people often ask whether buildings count as
extended phenotypes. T he answer is no, for the fates of the buildings
do not typically affect the fitness of the architects responsible. Extended
phenotypes only count if their variation is correlated with the success
of alleles responsible for that variation. This causal link exists for
beaver dams, but not for skyscrapers. Such a causal link is also what
sets extended phenotypes apart from niche construction. Niche con-
struction as a term was coined by John Odling- Smee (Odling-
Smee 1988; Odling-Smee et al. 2003), but it is perhaps best captured
by Levins and Lewontin in The Dialectical Biologist who wrote: ‘the
organism influences its own evolution, by being both the object of
natural selection and the creator of the conditions of that selection’
(Levins and Lewontin 1985, p. 106). Niche construction thus
encompasses all sorts of alterations of the environment by organisms.
That is, regardless of whether they are mere by- products of an
organism’s life cycle with no effect on its fitness or engineered
products with such effects. To proponents of niche construction (such
as Laland et al. 2016), extended phenotypes are a special case of the
former, whereas Dawkins considers the definition of niche construc-
tion to be so broad as to be useless (Dawkins 2004b; 2015, p. 336).
In part, this difference in opinion reflects the gene’s- eye view’s
stronger focus on explaining adaptations. In part, the attempt to
elevate niche construction theory is associated with a broader criticism
of much standard evolutionary theory. I am not going to adjudicate
that difference here. Papers in the Biology and Philosophy special issue
mentioned above (Dawkins 2004b; Laland 2004; Turner 2004;
Jablonka 2004) and the more recent exchange in The Journal of Genetics
(Gupta et al. 2017a, 2017b; Feldman et al. 2017) provide some flavour
of the kind of emotions that that debate elicits.
Even within the stricter definition of extended phenotypes, there
are plenty of examples of animal architecture. Mike Hansell documents
several of them and show that they typically fulfil one of three
functions: providing a secure home to live in, capturing prey, and
communicating with members of the same species (Hansell 2005).
Hansell’s comprehensive review demonstrate just how much is known
about how and why animals build. Yet, Dawkins (2004b) lamented
that twenty years after The Extended Phenotype, nobody had studied
the genetics of animal architecture.
A decade later, such a study finally appeared. Weber et al. (2013)
showed that the shape and size of the escape tunnels used by oldfield
mice (Peromyscus polionotus) are associated with a surprisingly small
number of genes. Using a quantitative trait locus mapping approach,
they identified four independent regions of the genome, each on a
different chromosome, that varies with variation in the tunnel
phenotype. One genomic region correlates with whether an individual
builds a tunnel at all, and three control the size of the tunnel, each
responsible for about 3 centimetres of length. The study beautifully
illustrates how the gene’s-eye view re-imagines the boundary between
organism and environment. Just as the environment is not restricted
to the outside of the organism, the phenotypic effects of a gene are
not limited to the organism itself.
Dawkins’s second kind of extended phenotype, action at a distance,
refers the manipulation of behaviour by another individual, of the
same or different species. T o Dawkins, the theoretical underpinnings
of action at distance can be traced to a paper he co-authored with
John Krebs on animal signals (Dawkins and Krebs 1978; see also Krebs
and Dawkins 1984). In it, they reject the field’s previous interpretation
of animal signals as always being cooperative, where cooperation is
aided by shared information. As an alternative hypothesis, they argued

that many signals are best thought of as attempts to manipulate the
behaviour of the receiver. T he idea of manipulation per se was not
new (already Aristotle knew about the brood parasitism of the
European Cuckoo; Schulze-Hagen et al. 2008), but the paper was part
of the general shift towards an increased focus on conflict in the study
of social behaviour.
Action at a distance may take many shapes and forms. One is that
of brood parasitism in birds, which occurs when a bird lays its eggs in
the nest of another individual (Davies 2000). Brood parasites reap the
rewards of parental care, including incubation and care of nestlings,
without having to pay the associated costs. Brood parasitism, which
occurs in about 1% of bird species, often takes ingenious forms. A
parasitic mother keeps a close eye on the host’s nest, making sure that
her timing is exactly right to sneak her eggs in. The parasite eggs
often closely resemble those of the host, and after hatching, the chicks
exploit their host parents in several ways. For example, hatchlings of
the European Cuckoo eject host eggs from the nest, leaving the host
with nothing but cuckoo eggs. Because the host, often a Gardner
Warbler or Reed Warbler, is much smaller, this results in the striking
situation in which the young cuckoo quickly grows larger than its
foster parent. Hosts are not completely helpless; they are often involved
in a co- evolutionary arms race with the parasites, resulting in
impressive changes to the colour and patterning of eggs (see Jamie 2017
for an excellent overview). Current research continues to reveal
surprising results about avian brood parasitism. Its genetic architecture,
however, remains poorly understood.
The situation is different in the third category of extended
phenotypes: parasites manipulating the behaviour of the host in which
they reside. This category shares many features with action at a distance
but differs in that the manipulator is located inside of the individual
being manipulated. T he experimental tractability of microorganisms
have meant that researchers have been able to identify a parasite gene
involved in causing the change in behaviour of a host. Healthy
c aterpillars of the European gypsy moth spend most of their days in

the soil to avoid predation, only venturing into trees to feed on leaves
at night. When they are infected by the baculovirus (Lymantria dispar
nucleo-polyhedrovirus), however, they climb to the treetop, where
they die, liquefy, and release the viral particles. T
his behavioural shift,
Hoover et al. (2011) elegantly demonstrated, is caused by the egt gene
of the virus.
As dramatic as this viral manipulation of gypsy moth behaviour
may seem, it is far from unique. Similar stories have been reported in
a wide variety of systems (Moore 2002; Hughes et al. 2012). One
striking example is that of rats infected by Toxoplasma gondii. These
rats lose their usual fear of cats, even developing an attraction to the
urine of their wonted predator. Once eaten, the parasite moves from
the rat to the cat, where it settles down and mates (Berdoy et al. 2000).
Another is that of zombie ants (Hughes et al. 2011; Fredericksen et
al. 2017). The fungal parasite Ophiocordyceps unilateralis infects the
carpenter ant host Camponotus castaneus and initially behaves similarly
to the baculovirus in the gypsy moth. It starts by making the ant move
away from the safety of its nest to a part of the plant that exposes the
ant but that has the right conditions for fungal growth. T he process
culminates with the fungus growing a long stalk straight through the
head of the ant. Because the stalk is topped with a bulb full of spores,
this allows the fungus to spread further.
Adopting a gene’s- eye view helps make sense of these bizarre
behaviours. A gene will be selected for even if the selected effects are
outside of the body in which the gene is located. T hey also illustrate
how proponents of the gene’s-eye view wants to rebuild the concept
of an organism: not as a physical body, but as ‘an entity, all whose genes
share the same stochastic expectation of the future’ (Dawkins 1990).
Host and parasite genes are in a way part of the same body, as they
reside in the same physical structure, but they have different
expectations of the future. Genes of vertically transmitted commensal
microbes have expectations better aligned with those of their host
organisms. Ever more so, that genes of the same genome share the
same expectation is often taken for granted, but two examples,

greenbeard genes and selfish genetic elements, show why that is not
necessarily the case.
5.3 Greenbeards
The concept of greenbeards is one of the most successful memes of

the gene’s-eye view and a salient example of how new theory identifies
new phenomena (Grafen 1998). The name itself comes from a
thought-experiment first presented by Hamilton (1964b) and then
developed and given its current name by Dawkins in The Selfish Gene
and in The Extended Phenotype (Dawkins 1976, pp. 115–116, 1982a,
pp. 143–155). T o Hamilton, the thought experiment was a way to
demonstrate that his concept of inclusive fitness was broader than the
process now known as kin selection.
Following Dawkins, a greenbeard is usually defined as a gene, or set
of closely linked genes, that has three effects (Gardner and West 2010;
West and Gardner 2010; Madgwick et al. 2019):
1. It gives carriers of the gene a phenotypic label, such as a green

beard.
2. The carrier can recognize other individuals with the same label.
3. The carrier then behaves nepotistically towards individuals with
the same label.
Dawkins’s presentation of Hamilton’s insight is striking, but its

cartoon-like character obscures some of the general properties of the
greenbeard effect. For example, the phenotypic marker (the green-
beard) is not required. T he key feature is that the gene for social
behaviour is linked to the genetic basis of the assortment mechanism,
which can happen if the genes for nepotistic behaviour and habitat
preference are linked (Hamilton 1975). For example, if the greenbeard
locus makes individuals follow a certain flower scent and then behave
nepotistically towards other individuals at that flower (Madgwick

et al. 2019).
The greenbeard effect should be distinguished from what Dawkins
called the ‘armpit effect’ (Dawkins 1982, p. 146). The latter refers to
situations where an organism recognizes a trait (like odour) in itself,
or in a close relative, and then favours other individuals with the same
trait. As such, it provides a mechanism for traditional kin-recognition.
Greenbeard genes work to recognize copies of themselves, not of kin.
This is also why the armpit effect is expected to be mediated by high
genome-wide relatedness, whereas the greenbeard effect relies only
on high relatedness at the locus/loci underlying it.
5.3.1 Why greenbeards should be rare in nature

The conditions for their existence meant that greenbeards were long
thought to be unlikely to exist in nature (Dawkins 1978, 1979;
Grafen 1984). Madgwick et al. (2019) group arguments for why
greenbeards should be rare in natural populations into three categories:
existential, detection, and selection arguments.
The existential argument points out that greenbeards rely on the
assumption that a single gene, or a set of tightly linked genes, can
affect all three phenotypic functions required. This seems unlikely,
especially as the connection of genotype to phenotype will need to
be deterministic, or close to deterministic. Combined, these improb-
able conditions mean that greenbeards should evolve only very
rarely (West et al. 2007). In response, Haig has noted that there are
several examples of genes, or sets of closely linked genes, that can
recognize themselves in others, including mechanisms like cell–cell
receptors (Haig 1996, 2013). Furthermore, a greenbeard gene does
not need to directly cause the traits; it can achieve its effect by
adjusting the expression of other genes. The kinds of phenotypes
that can be regulated in this way may be limited, which could
explain why many of the best examples of greenbeards come from
microbes, whose simpler genetic architectures can prevent pleiotropic
traits from being broken up, ensuring that beards and behaviour
stay linked.
The detection argument holds that even if greenbeards do evolve,
they will be difficult for researchers to notice in nature. T he reason for
this is that greenbeard genes are expected to evolve under strong
selection and so will rapidly spread to fixation in the population
(Biernaskie et al. 2013). At that point, the greenbeard would lose its
effect. There seem to be biological reasons for why this does not
always happen. T ake, for example, the Gp-9 greenbeard gene in the
red fire ant (Solenopsis invicta), the first example of a greenbeard found
in nature (Keller and Ross 1998; Ross and Keller 2002). Gp-9 is
involved in the production of an odour-binding protein and comes in
two alleles (B and b). The recessive allele (b) acts as a greenbeard by
causing workers to use the odour to detect queens that lack the allele
and kill them. Queen-killing can happen because the queens in pop-
ulations with multiple queens are heterozygous (Bb) at the Gp-9 locus.
These Bb queens produce BB and Bb offspring (bb offspring die
young). BB queens would give rise to mongyne colonies (i.e. with
only one queen), were they not killed by Bb workers. The homozy-
gous lethality means that b will not spread to fixation, and the result-
ing polymorphism is what allows the greenbeard to be detected.
Another reason that greenbeards may be difficult to detect is that
they may be in conflict with the rest of the genome (Alexander and
Borgia 1978). Such a situation arises when the relatedness coefficient
between two individuals at the greenbeard locus is different from the
genome-wide average. Whereas it is in the interest of the greenbeard
locus to favour another greenbeard individual, this interest may not be
shared by other genes in the genome. For some time confusion existed
in the literature about the generality of this situation. For example,
Ridley and Grafen (1981) demonstrated that a suppressor mutation
that prevents the greenbeard from being expressed will generally be
favoured only when the greenbeard itself is under positive selection.
While suppressing the greenbeard saves the individual the cost of
behaving favourably towards other greenbeards, the suppression also
prevents the individual from reaping the rewards of receiving altruistic

acts from other greenbeards. Ridley and Grafen further argued that if
a suppressor could keep the beard while simultaneously suppressing
the altruistic act, this false-beard situation would create the stage for
conflict. Biernaskie et al. (2011) clarified the situation by developing
models of greenbeards and false beards with and without suppressors.
They showed that the fitness interests of greenbeards will generally be
in line with the rest of the genome. The exception, conflict, occurs
when a greenbeard individual is interacting with closely related kin.
Here, kin selection will favour altruistic behaviour towards all close
relatives, but the greenbeard locus will be selected to restrict it to
fellow greenbeards.
Finally, the selection argument is that greenbeards are unlikely to be
selected for to begin with. Because the benefit of having a beard is
only realized when there are other beards around, several mathematical
models have shown that greenbeards may struggle to increase at low
frequencies (Jansen and van Baalen 2006; Gardner and West 2010;
Biernaskie et al. 2011).While limiting the opportunity for greenbeard
genes to invade a population, demographic factors like population
structure can readily provide the right circumstances. Although new
greenbeard mutations will be rare in the general population, they may
be locally common within a kin group.
5.3.2 Helping and harming greenbeards

Despite the expectation that greenbeards should be rare in natural
populations, several examples have been identified. One particularly
well-researched example is that of clumping in yeast (Saccharomyces sp.;
reviewed in El-Kirat-Chatel et al. 2015). In response to stress, thousands
of yeast cells come together to form large clumps (‘flocs’) that resemble
bacterial biofilms. This cooperative behaviour provides protection
from various environmental stressors, including anti- microbial
substances and ethanol, as cells on the inside of the floc are physically
shielded from the external environment. The protection, however,
comes with a fitness cost, which has been demonstrated by growing

flocculating and non-flocculating cells under non-stressful conditions.
In such a benign environment, non-flocculating cells grow four times
faster than flocculating cells. Flocculation has been used for centuries
in the brewing industry to remove excess yeast during alcohol
production, but it is typically absent in lab strains (Speers 2012).
The genetics of flocculation has also been extensively studied.
Smukalla et al. (2008) identified the flocculating gene FLO1 as a
greenbeard locus in S. cerevisiae. The FLO1 locus produces a trans-
membrane protein that allows yeast cells to bind to one another. Cells
that share the cooperative FLO1 allele flocculate together, while those
that lack the cooperative allele are mostly excluded from flocs. T he
tractability of the FLO1 system offers an excellent opportunity to
experimentally teach students which aspect of inclusive fitness the-
ory–kin selection or the greenbeard effect–best explains a cooperative
behaviour, as thousands of undergraduates at the University of Toronto
have come to experience (Ågren et al. 2017).
The Gp-9 and FLO-1 examples differ both in the nature of their
host organism and in the way that the greenbeard effects comes about.
In his original popularization of the concept, Dawkins outlined a
scenario where greenbeards help fellow greenbeards (Dawkins 1976,
pp. 115–116, 1982, pp. 143–155). This is what happens in the FLO-1
example and also when slime mould (Dictyostelium discoideum)
individuals with the same csa allele stick together in fruiting bodies,
excluding individuals with other alleles (Queller et al. 2003). In
contrast, the queen killing in the red fire ant is an example of a
greenbeard effect that is achieved by greenbeards actively harming
non-greenbeards. Greenbeards can therefore generally be divided into
‘helping’ and ‘harming’ greenbeards (Gardner and West 2010).
Additional examples of each kind have been described, including
helping greenbeards in the fungus Neurospora crassa (Heller et al. 2016)
and the marine tunicate Botryllus schlosseri (De Tomaso 2018). Bacteria
seem to have examples of both helping and harming greenbeards
(Riley and Wertz 2002; Pathak et al. 2013).
These empirical examples combine with theoretical advances

connecting the evolutionary dynamics of greenbeards to everything
from the evolution of warning coloration (Guilford 1985) to sexual
selection (Faria et al. 2018), to transform what was once a cute amusing
thought experiment into chloropogonology (Gardner and West 2010),
the thriving study of greenbeards. Relevant to the gene’s-eye view,
greenbeard genes highlight how the oft-assumed unity of p urpose of
the genome can break down. The potential for such breakdown is
even greater in situations involving selfish genetic elements.
5.4 Selfish genetic elements
Traditionally, the predominant view of genomes was that of a highly

coordinated network, with all parts working together for the same
purpose. Genetic transmission was assumed to be fair and to be
governed by the rules laid out by Mendel. The traditional view is
challenged by the existence of stretches of DNA that can subvert
these rules and promote their own transmission at the expense of
other parts in the genome, with either no or a negative effect on
organismal fitness. Such stretches of DNA are now usually called
selfish genetic elements, but they have previously been known as
parasitic DNA, selfish DNA, ultra-selfish genes, genomic outlaws,
and self-promoting elements (reviewed in Werren et al. 1988; Burt
and Trivers 2006; Werren 2011; Gardner and Úbeda 2017; Ågren and
Clark 2018).
5.4.1 Early work on selfish genetic elements

Though foreshadowed by T.H. Huxley’s ideas about competition
among gemmules (Huxley 1878), proper discussions of selfish genetic
elements began in earnest a few decades later. In 1928, the Russian
geneticist Sergey Gershenson reported the discovery of a driving X
chromosome that was inherited in more than 50% of the gametes in
Drosophila obscura (Gershenson 1928). Crucially, he noted that the

resulting female-biased sex ratio could potentially drive a population
extinct. Haldane discussed several examples of conflict between
different levels in the biological hierarchy, including how pollen
competition could lead to the spread of traits that were deleterious to
the individual plant (Haldane 1932, p. 67). In 1945, the Swedish botanist
and cytogeneticist Gunnar Östergren argued that supernumerary
(i.e. non-vital) B chromosomes were best conceived as parasitic
(Östergen 1945). Östergren’s paper was the first unambiguous
articulation of the idea of selfish genetic elements.
Östergren’s work coincided with several similar observations,
particularly in plants (Ågren and Wright 2015). For example, female
meiotic drive was first reported in maize (Rhoades 1942), and Lewis
(1941) presented evidence that cytoplasmic male sterility in plants
resulted from the conflict between maternally inherited organellar
and biparentally inherited nuclear genes. T hen, in the early 1950s,
Barbara McClintock published a series of papers describing the exist-
ence of transposable elements, which are now recognized to
be among the most successful selfish genetic elements there are
(McClintock 1950, 1956; though McClintock herself rejected the
selfish label). Her discovery of transposable elements led to the Nobel
Prize in Medicine or Physiology in 1983 and she remains the only
woman to have been awarded the prize on her own. These examples
were initially considered to be genetic oddities with few implications
for evolutionary theory (Burt and Trivers 2006, pp. 12–16;Werren 2011).
It would take several decades before selfish genetic elements in general,
and their evolutionary implications in particular, became widely
appreciated.
The gene’s-eye view played an important role in bringing selfish
genetic elements to the high table of genetics and evolutionary
biology.Viewing evolution as a struggle between competing replicators
made it easier to recognize that not all genes in an organism would
share the same evolutionary fate (Rothstein and Barash 1983). As
Dawkins put it:
It is a remarkable fact that natural selection seems to have chosen those

replicators that cooperate with each other and go around in the large
collective packages which we see as individual organisms. T his is a fact
that needs explaining in its own right, just as the existence of sexual
reproduction needs explaining in its own right. (Dawkins 1978)
In addition to the general conceptual shift to gene-level thinking in

evolutionary biology, empirical observations also led the way in the
origin of the study of selfish genetic elements (Werren 2011). Early
work on genome structure reported that large chunks of eukaryotic
genomes were made up of genetic material, such as repetitive DNA,
with seemingly no connection to organismal function or fitness (see,
e.g., Britten and Kohne 1968). Moreover, while it was clear that
genome size varies dramatically across species (it is now known that
eukaryotes vary more than 60,000-fold; Elliott and Gregory 2015),
there was no correlation between the amount of DNA in an organism
and its perceived complexity. For example, the genome of a single-
celled amoeba is about 100 times larger than that of humans.
These accumulating empirical observations were central to two
papers published back-to-back in Nature in 1980, by Leslie Orgel and
Francis Crick, and Ford Doolittle and Carmen Sapienza respectively.
Both papers attempted to counter the prevailing view of the time that
the presence of differential amounts of non- coding DNA and
transposable elements was best explained from the perspective of
individual fitness, described as the ‘phenotypic paradigm’ by Doolittle
and Sapienza. T he authors argued that much of the genetic material
in eukaryotic genomes persists, not because of its phenotypic effects,
but, citing Dawkins, that it can be understood from a gene’s-eye view
without invoking individual-level explanations. T hese papers resulted
in a series of exchanges in Nature (Dover 1980; Cavalier-Smith 1980;
Orgel et al. 1980; Dover and Doolittle 1980; Jain 1980) representing
the first high profile discussion of the evolutionary implications of
selfish genetic elements.
These papers marked the beginning of the serious study of selfish
genetic elements, and the subsequent decades saw a rapid increase in
both theoretical advances and empirical discoveries. Leda Cosmides

and John Tooby wrote a landmark review about the conflict between
maternally inherited organellar genes and biparentally inherited
nuclear genes (Cosmides and Tooby 1981; see also Eberhard 1980).
Their paper used the gene’s-eye view to provide a comprehensive
introduction to the logic of genomic conflicts, foreshadowing many
themes that would later become research foci. In 1988, Jack Werren
and colleagues wrote the first major empirical review of the topic
(Werren et al. 1988). In it, they coined the term selfish genetic
element, putting an end to the confusingly diverse terminology
mentioned above. It was also the first paper to bring together all
the different kinds of selfish genetic elements known at the time, dis-
cussing examples ranging from meiotic drive and supernumerary B
chromosomes to killer plasmids, selfish mitochondria, and transposable
elements.
In the 1980s, selfish genetic elements seem to have been considered
an exception of limited interest. By 2006, when Austin Burt and
Robert Trivers published the first book-length treatment of the topic,
a comprehensive piece that remains the go-to source, the tide was
changing. While the role of selfish genetic elements in evolution long
remained controversial, a recent review concluded with a statement
that no longer feels particularly radical: ‘nothing in genetics makes
sense except in the light of genomic conflicts’ (Rice 2013).
5.4.2 Examples of selfish genetic elements

Selfish genetic elements have now been described in most groups of
organisms, and they demonstrate a remarkable diversity in the ways
they promote their own transmission. Below, I discuss some examples
of this diversity.
Genomic conflicts often arise because not all genes are inherited
in the same way. Probably the best example of this is the conflict
between uniparentally (usually, but not always, maternally) inherited
mitochondrial and biparentally inherited nuclear genes (Havird et al.
2019; Ågren et al. 2019b). T he conflict between mitochondrial and

nuclear genes is especially well-studied in flowering plants. Flowering
plants are typically hermaphrodites and mitochondrial genes are
usually only transmitted through female gametes. From their point of
view, the production of pollen leads to an evolutionary dead end. Any
mitochondrial mutation that can affect the amount of resources the
hermaphroditic plant invests in the female reproductive functions at
the expense of the male reproductive functions improves its own
chance of transmission. Cytoplasmic male sterility, then, is the loss of
male fertility, typically through loss of functional pollen production,
resulting from a mitochondrial mutation (Case et al. 2016). In many
species where cytoplasmic male sterility occurs, the nuclear genome
has evolved so-called restorer genes, which repress the effects of the
cytoplasmic male sterility genes and restore the male function, making
the plant a hermaphrodite again.
Mito-nuclear conflict in plants is a good example of the strength
and limitations of the gene’s-eye view. It provides a clear logic as to
why transmission asymmetries should result in genomic conflicts. At
the same time, it has little to offer on the question why there are no
reported examples of conflict between nuclear and chloroplast genes,
which like mitochondrial genes are usually uniparentally inherited.
A related consequence of the maternal inheritance of the
mitochondrial genome is the so-called Mother’s Curse. T his is the
name given to the fact that because genes in the mitochondrial
genome are strictly maternally inherited, mutations that are beneficial
in females can spread in a population even if they are deleterious in
males (Gemmell et al. 2004). A key observation consistent with this
idea is that mitochondrial genetic disease in humans seem to affect
males more than females (Frank and Hurst 1996). Explicit screens in
fruit flies have also successfully identified female-neutral but male-
harming mitochondrial mutations (Camus et al. 2012; Patel et al. 2017).
In humans, a 2017 paper studying the prevalence of Leber’s hereditary
optic neuropathy, an eye disease, in Quebec, Canada, showed how the
mutation causing the disease is present at an unusually high frequency
given the severity of the syndrome. The way to make sense of this is
that the disease-causing mutation is located in the mitochondria and
that the disease affects males more than females (Milot et al. 2017). In
an extra twist to the story, the authors were able to demonstrate that
the mutation was introduced to the Quebec population by one of the
so-called Filles du roi (King’s Daughters) who were sent there in the
17th century by the French King Louis XIV in an attempt to help
populate the colony of New France.
Another way that selfish genetic elements can manipulate the
transmission to their own advantage is to interfere directly with the
process of meiosis. Because sexual reproduction results in a zygote
that is the product of the mixing of genes from two individuals, an
opportunity for competition between nuclear genes in each parent
arises over who makes it into the zygote. T his potential conflict is
mainly avoided by the imposition of fair meiosis (Leigh 1971; Haig
and Grafen 1991; Frank 2003). Still, there are several ways genes can
cause unfair meiosis and end up being overrepresented in gametes
(Lindholm et al. 2016). One example from female meiosis involves
genes that ensure that they are preferentially transmitted to the egg
cell, as opposed to one of the two polar bodies. Because polar bodies
are not fertilized, genes with this ability are guaranteed to be
transmitted to the next generation. Another example are so-called
sperm killers, where genes damage the development of sperms in
which they are absent. Two of the best studied examples of this selfish
strategy are the Segregation Distorter in Drosophila melanogaster
(Larracuente and Presgraves 2012) and the t-haplotype of the domestic
mouse Mus musculus (Herrmann and Bauer 2012).
A closely related example is B chromosomes. T hese are chromo-
somes that are not required for the viability or fertility of the organ-
ism but exist in addition to the normal set (the so-called A set;
Jones 1991; Douglas and Birchler 2017; Benetta et al. 2019). B chro-
mosomes persist in the population and accumulate because they have
the ability to propagate themselves faster than the A chromosomes.
Though typically smaller than other chromosomes, their gene poor,
heterochromatin-r ich structure made them visible to early cytogenetic

techniques and B chromosomes were first detected over a century
ago (Wilson 1907; see also Östergren 1945). They have been thor-
oughly studied and are estimated to occur in 15% of all eukaryotic
species (Beukeboom 1994) and appear to be particularly common
among eudicot plants, while rare in birds and mammals. T he pheno-
typic consequences of B chromosomes are unclear, but copy number
correlates positively with genome size (Trivers et al. 2004) and has
also been linked to a decrease in egg production in grasshoppers
(Zurita et al. 1998).
A kind of selfish genetic element that has received a lot of attention
in recent years are homing endonucleases. These are enzymes that cut
DNA in a sequence-specific way, and those cuts are then ‘healed’ by
the regular DNA repair machinery (Burt et al. 2004; Belfort and
Bonocora 2014). Because homing endonucleases cause these cuts at
the site homologous to the first insertion site, this results in a conversion
of a heterozygote into a homozygote. CRISPR- Cas9 technology
allows the artificial construction of homing endonuclease systems, so-
called ‘gene drive’ systems. Gene drives have the potential to introduce
a desired allele in a population, with the ability, for example, to
exterminate malaria-carrying mosquitos, and so present a combination
of great promise for biocontrol and risk to ecosystem dynamics (see
discussions by, e.g., Esvelt et al. 2014 and Champer et al. 2019).
The most successful kind of selfish genetic element, at least in terms
of abundance, are transposable elements. This group includes a wide
variety of DNA sequences that all have the ability to move to new
locations in the genome of their host. DNA transposons do this by a
direct cut-and-paste mechanism, whereas retrotransposons need to
produce an RNA intermediate to move, analogous to a copy-and-
paste mechanism. Regardless of the specific mechanism of self-
replication, most transposon insertions appear to be relatively
innocuous (Lisch 2013). For example, the colour difference between
the wine grapes of Cabernet, Chardonnay, and Ruby Okuyama are
due the insertion (Cabernet to Chardonnay) and subsequent loss
(Chardonnay to Ruby Okuyama) of a specific retrotransposon.

Genomes also seem fairly tolerant of the presence of transposons in
their genomes. A sizable portion of the genome of many animals and
plants is made up of transposons, including some 50% of the human
genome and more than 80% of that of maize (Tenaillon et al. 2010;
Kapusta et al. 2017).
The movement of transposons is also a source of mutations, some
with devastating results. For example, the presence of transposons have
been linked to human diseases ranging from cancer to haemophilia
(Hancks and Kazazian 2016). Both plants and animals have therefore
evolved means for reducing the deleterious fitness consequences of
transposable elements, often through quite intricate small RNA inter-
ference mechanisms (Blumenstiel 2011; Kelleher et al. 2020). Because
new insertions can disrupt gene function, sometimes those changes
can have positive fitness effects, just like any other kind of mutation.
Examples of transposon-driven adaptive changes range from Drosophila
(Aminetzach et al. 2005) to dogs (Cordaux and Batzer 2006), but the
most charismatic example is probably the discovery that the mutation
underlying the industrial melanism in the peppered moth is a transpos-
able element insertion (van’t Hof et al. 2016).
5.4.3 Two rules for selfish genetic elements

Though selfish genetic elements demonstrate a tremendous diversity
in how they alter the rules of transmission to promote their own
interests, some commonalities can be identified. In a 2001 review,
Greg Hurst and Jack Werren proposed two such ‘rules’ for selfish
genetic elements (Hurst and Werren 2001). Both demonstrate the
power of the gene-centred thinking.
Their first rule is that selfish genetic elements need sex to spread. In
asexual lineages, selfish genetic element are essentially stuck, as the
same genome is passed on intact from parent to offspring. This will
increase the variation in fitness among individuals, resulting in stronger
purifying selection in asexually reproducing lineages, for a lineage
without the selfish genetic elements should outcompete a lineage

with the selfish genetic element. Sex, in contrast, allows selfish genetic
elements to spread into new genetic lineages. In line with this, popu-
lation genetic theory generally predicts the absence of sex is expected
to lead to a reduction in the number of selfish genetic elements pre-
sent in the genome (Hickey 1982; Wright and Schoen 1999; Dolgin
and Charlesworth 2006).
An important caveat to this prediction is that the efficacy of
selection is expected to be reduced in asexual lineages due to the low
rates of recombination. Such a reduction may result in the accumulation
of deleterious mutations, which includes most selfish genetic elements,
in a process known as a Muller’s ratchet (reviewed in Hartfield 2015).
Mathematical modelling has shown that asexual lineages may be
driven to extinction through an indefinite accumulation of transposable
elements (Hickey 1982; Dolgin and Charlesworth 2006). Many of the
predictions about the abundance of selfish genetic elements in sexual
versus asexual lineages also apply when comparing self-fertilizing and
outcrossing lineages.
To date the empirical evidence for the importance of sex and
outcrossing comes from a variety of selfish genetic elements. Examples
include finding a higher abundance of self-promoting plasmids in
sexual compared to asexual yeast strains (Harrison et al. 2014) and
more B chromosomes in outcrossing than self-fertilizing plants (Burt
and Trivers 1998). For transposable elements, the results are mixed.
Studies in plants (Ågren et al. 2014), animals (Bast et al. 2016; Szitenberg
et al. 2016), and fungi (Bast et al. 2019) have reported differences in
both directions and neither.
The second rule is that hybrids are often required to reveal the
presence of selfish genetic elements in a population. There are two
key reasons for this. First, selfish genetic elements can rapidly sweep to
fixation. Unless a specific element is segregating in the population, so
that some individuals carry it and others do not, its presence is very
difficult to detect. Hybridization events, however, may produce
offspring with and without the specific selfish genetic elements and
so reveal their presence. Second, host genomes have evolved

mechanisms to suppress the activity of the selfish genetic elements.
Examples include the silencing of transposable elements by small
RNAs and nuclear genes that restore male fertility in the face of selfish
mitochondria. If the co-evolution of selfish genetic elements and
their suppressors is rapid, that can also mask the presence of selfish
genetic elements in a population. Hybrid offspring, on the other
hand, may inherit a selfish genetic element but not its corresponding
suppressor and so reveal its presence.
Co-evolution between selfish genetic elements and their suppressors
can also cause reproductive isolation through so- called Bateson–
Dobzhansky–Muller incompatibilities (Crespi and Nosil 2013;
Ågren 2013; Serrato-Capuchina and Matute 2018). An early striking
example of hybrid dysgenesis induced by a selfish genetic element is the
P element in Drosophila melanogaster (Kidwell 1983).When males carry-
ing the P element were crossed to females lacking it, the resulting off-
spring suffered from reduced fitness, whereas offspring of the reciprocal
cross were normal (this is expected because piRNAs are maternally
inherited). T he P element is typically present only in wild strains, not in
the lab strains of Drosophila melanogaster that were collected before the P
elements became widespread in the species. Recently the P element has
invaded natural populations of the closely related D. simulans, where it
is also causing hybrid dysgenesis (Kofler et al. 2015; Hill et al. 2016).
The P element story is a good example of how the rapid co-
evolution of selfish genetic elements with their silencers can quickly
lead to incompatibilities in as little as a few decades. Several other
examples of selfish genetic elements causing reproductive isolation
have since been demonstrated. Hybrid dysgenesis has been shown to
be associated with centromeric drive in barley (Sanei et al. 2011), sex
ratio distorters in flies (Verspoor et al. 2018), and in several species
of flowering plants by mito–nuclear conflict (Rieseberg and
Blackman 2010). After much initial skepticism regarding the potential
role of selfish genetic elements in speciation (reviewed in Patten 2018),
attitudes in the field seem to be changing.
5.4.4 Selfish genetic elements and selfish genes

In an interview with Ullica Segerstrale, Robert Trivers said ‘I will get
Lewontin at the molecular level!’ (Segerstrale 2000, p. 330). In addition
to being a long-term critic of the gene’s-eye view, Lewontin had also
been at the forefront of bringing molecular data into evolutionary
analysis (e.g. Hubby and Lewontin 1966; Lewontin and Hubby 1966).
Trivers, in contrast, had been instrumental in the origin of the
emergence of the gene’s-eye view and was one of the first to see the
conceptual complementarity of selfish genetic elements and selfish
genes in the more general Dawkinsian sense. Together with Austin
Burt, with whom he began writing Genes in Conflict in the early
1990s (Burt and Trivers 2006, p. vii), he had a particularly good under-
standing of the significance of the molecular data on selfish genetic
elements. T o Trivers, the abundance of data on selfish genetic ele-
ments would provide the ultimate vindication of the superiority of
the gene’s-eye view.
The relationship between the gene’s-eye view and the study of
selfish genetic elements may in retrospect seem straightforward. Just
consider the similarity in language in two key papers in each field:
Hamilton’s first paper, the 1963 note in the American Naturalist and
Östergren’s 1945 paper on B chromosomes mentioned above:
Despite the principle of ‘survival of the fittest’ the ultimate criterion
that determines whether [a gene for altruism] G will spread is not
whether the behavior is to the benefit of the behaver but whether it is
of benefit to the gene G. (Hamilton 1963)
In many cases these chromosomes have no useful function at all to
the species carrying them, but that they often lead an exclusively para-
sitic existence . . . [B chromosomes] need not be useful for the plants.
They need only be useful to themselves. (Östergren 1945)
A crucial conceptual insight in both papers is that in order to explain

the phenomenon under study, the origin of altruism and the spread of
B-chromosomes respectively, the investigator is better off viewing the
world from the perspective of genes rather than individual organisms.
While the evolutionary logic of altruism and selfish genetic elements

is difficult to follow from an organismal perspective, it is straightforward
from a gene’s-eye view.
The existence of selfish genetic elements has often been seen as one
of the strongest arguments for the approach (Okasha 2006, p. 153,
2012; Ågren 2016; Ridley 2016; De Tiège et al. 2018). For example,
when discussing the work of Eberhard (1980) and Cosmides and
Tooby (1981) on the conflicts between the nuclear and organellar
genomes, Dawkins (1982a) wrote: ‘Neither Eberhart nor Cosmides
and Tooby explicitly justify or document the genes’-eye view of life:
they simply assume it (…) These papers have what I can only describe
as the flavour of post-revolutionary normal science’ (Dawkins 1982a,
p. 178). This is not the whole story, however. In Adaptation and Natural
Selection, Williams discussed only one example of a selfish genetic
element, the t-haplotype in mice studied by Lewontin (Lewontin and
Dunn 1960; Lewontin 1962). Ironically, the inability of the t-haplotype
to spread to high frequencies is presented by Williams (1996, p. 117), as
well as by Leigh (1971, p. 247), as the only convincing case of group
selection in nature.
The tension between selfish genetic elements and other levels of
selection was also central to Gould’s argument for a hierarchical
approach to evolutionary theory. In The Structure of Evolutionary Theory,
he wrote:
When future historians chronicle the interesting failure of exclusive
gene selectionism (based largely on the confusion of bookkeeping
with causality), and the growing acceptance of an opposite hierarchical
model, I predict that they will identify a central irony in the embrace
by gene selectionists of a special class of data [selfish genetic elements],
mistakenly read as crucial support, but actually providing strong evi-
dence of their central error. (Gould 2002, p. 689)
How to make sense of Gould’s critique? One way is to recall the dis-
cussion of pluralistic gene selectionism in Chapter 3 and note several
versions of the gene’s-eye view can be said to exist. The strongest ver-
sion argues that the gene level is the only level of selection, and talking
about other levels is misleading. This is how much of The Selfish Gene
is written. Other, weaker, versions emphasize that the Necker cube
approach to genic and individual selection and/or suggest that all
instances of evolution can at least be represented as changes in allele
frequency. The least controversial version simply states that in some
cases, for example selfish genetic elements, the gene is the level of
selection.
Above Gould is attacking the strongest version of the gene’s-eye
view, the argument that only the gene level perspective truly represents
evolution by natural selection. Although he never warmed to the
term ‘selfish DNA’ (as selfish genetic elements were often called
during Gould’s active years), as he thought it privileged the individual
organism in an inappropriate way, he did consider selfish genetic
elements to be strong evidence for a hierarchical view of evolutionary
biology (Gould 1977, 1983a). The link between within- genome
selection and hierarchy was later been picked up and expanded

by several others (Vrba and Eldredge 1984; Doolittle 1989;
Gregory 2004, 2013; Gregory et al. 2016). The main argument of
these authors is that evolutionary explanations of selfish genetic ele-
ments must involve selection at both the level of the selfish genetic
element and at the level of the individual organism. Like proponents
of a gene’s-eye view, Gould and his intellectual allies strive to demote
the individual from a central position in evolutionary theory. T he two
groups part ways in that Gould and friends want to add additional
levels to the hierarchy, whereas gene selectionists insist on focusing on
one level, that of the gene.
Given Gould’s aversion for adaptationism, it is surprising that he
did not pick up on how the gene’s-eye view and the study of selfish
genetic elements can act to counter naive adaptationist thinking.
Instead, this message was deliver by two representatives of evolutionary
psychology, often considered the worst offenders of uncritical
adaptationism, Leda Cosmides and John Tooby. The pair made the
point in a sharply worded letter to the editor of The New York Review
of Books responding to two of Gould’s essays that touched on
evolutionary psychology (Gould 1997a, 1997b; the letter was rejected

but uploaded online, Tooby and Cosmides 1997). Together with
Jereme Barkow, Cosmides and Tooby were the editors of The Adapted
Mind: Evolutionary Psychology and the Generation of Culture (Barkow et
al. 1992), often considered the foundational text of the field. As noted
above, Cosmides and Tooby had also made a substantial contribution
to the study of genomic conflict with their 1981 paper (Cosmides and
Tooby 1981). A key point of their letter was that a gene’s-eye view
forces biologists to look beyond individual organisms to see the
amount of maladaptation caused by selfish genetic elements. Since
that letter, the appreciation of the phenotypic consequences, beneficial
and deleterious and neutral, of selfish genetic elements has increased
(Lisch 2013; Rice 2013), and it has become more difficult to ignore the
existence of competing genes within individuals when the goal is to
develop a general account of adaptation.
As discussed in Chapter 4, the idea that individual organisms act to
maximize their inclusive fitness is based on the assumption of genomic
unity of purpose. Selfish genetic elements show that not all genes share
the same fitness interests and rather than being a cohesive fitness maxi-
mizer, the individual organism is a compromise of several fitness inter-
ests. A recent paper set out to tackle this contradiction (Scott and
West 2019). T hey develop a series of mathematical models of selfish
genetic elements and suppressors to argue that selfish genetic elements
will either impose fitness costs that are too weak to be important, or, if
the fitness costs to the individual organism are large, they will be readily
suppressed. From this, they argue that even if selfish genetic elements
are common, their effects will be negligible and can be ignored, thus
maintaining the idea of individual level fitness maximization.
There are issues with this conclusion. As Scott (2019, p. 211) points
out there is an implicit bias in their approach that saves the individual.
They assume that the individual is already maximizing its fitness,
which results in a situation where a selfish genetic element cannot
push the individual away from that maximization. What they show is
not how fitness maximization can be achieved in the presence of
selfish genetic elements in the first place, but how it can be main-
tained once it is there.
5.4.5 The only game in town?

Just as trying to explain everything in terms of individual fitness makes
biologists ignore too much interesting biology, too much focus on
individual genes can also lead one astray. For example, those seduced
by the gene’s-eye view can overemphasize genomic conflict at the
expense of genomic cooperation (Wade and Drown 2016). How
genes cooperate has received much less attention than how whole
organism cooperate (Ågren 2014;Yanai and Lercher 2016).A noticeable
exception is research on cooperation in the RNA world (Higgs and
Lehman 2015), which is a potential empirical goldmine to be
approached with the tools of the gene’s-eye view.
The gene’s-eye view is arguably the most powerful way to think
about selfish genetic elements. It is, however, not the only way.
Additional frameworks highlight other aspects of their biology. T o date,
conceptual and empirical insights have come from several traditions
including, but not limited to, multi-level selection theory (Gregory
2013; Gregory et al. 2016), host–parasite interactions (Nee and Maynard
Smith 1990; Hurst 1996; Brookfield 2011), political philosophy
(Okasha 2012), epidemiology (Wagner 2009), and community ecology
(Venner et al. 2009; Linquist et al. 2015). All frameworks are not created
equal, but most can contribute something. Studying of selfish genetic
elements is difficult; we need all the help we can get.
5.5 Summary
• The emergence of the gene’s-eye view led or contributed to the

development of several new empirical research avenues. Chief
among these were the study of extended phenotypes, greenbeards,
and selfish genetic elements.
• Extended phenotypes include ‘all the effects that a gene causes on

the world’ and can be grouped into three main categories: animal
architecture, action at a distance, and parasite manipulation of host
behaviour.
• Greenbeard genes are genes that can identify copies of themselves
in other individuals and then make their carrier act nepotiscally
towards those individuals or selfishly towards non- carriers. The
term comes from a thought experiment meant to demonstrate that
from a gene’s perspective, what matters is the relatedness at a
particular locus that causes the social act, not the average relatedness
across the genome. Although initially the conditions for their
existence were thought to be too restrictive, many examples of
greenbeard genes have been identified in natural populations.
• Selfish genetic elements have the ability to promote their own
transmission despite having a harmful effect on the fitness of the
individual organism. They come in a remarkable diversity of fla-
vours and they are a prominent feature of nearly all sexually repro-
ducing organisms.
• In their own ways, extended phenotypes, greenbeards, and selfish
genetic elements, all highlight the value of thinking from a gene’s
perspective, and strengthen the gene’s- eye view’s attempt to
dethrone the individual organism as the central unit of explanation
in evolutionary biology.
Conclusion: The Gene’s-Eye

View Today
M arian Stamp Dawkins once recounted her experience marking

a final exam paper by one of her undergraduates (Stamp
Dawkins 2006).The student successfully answered the set question on
how natural selection could have resulted in some animals not repro-
ducing, using all the correct technical terms, but then went on to say
‘And here I rely heavily on the words of Richard Dawkins’ before
wrapping up their conclusion. In response, Stamp Dawkins noted in
the margin of the examination paper: ‘Yes. Don’t we all?’
There is no denying that for the past decades the field of evolution-
ary biology—students and faculty alike—have relied much on the
words of Richard Dawkins. As this book has shown, people disagree
whether this is a good thing or not.
In The Descent of Man, Darwin distinguished between ‘false facts’
and ‘false views’ (Darwin 1871, p. 385). False facts, he argued, were
directly detrimental to the progress of science as they had a tendency
to linger on. In contrast, false views that had some empirical support,
could actually be beneficial to a field, as ‘every one takes a salutary
pleasure in proving their falseness’. Always one for coining a catchy
phrase, Gould christened these kinds of views that were incorrect, but
nevertheless fruitful, Pareto errors, after the economist Vilfredo Pareto
who is meant to have said: ‘give me the fruitful error any time, full of
seeds, bursting with its own corrections. You can keep your sterile
truth for yourself ’ (quoted in Gould 2002, p. 612).
DOI: 10.1093/oso/9780198862260.003.0007
conclusion: T h e ge n e’s-ey e v i ew today 181
To Gould, there was no bigger Pareto error in evolutionary biology

than the gene’s-eye view. T
his book is my answer to Gould’s accusation.
The gene’s-eye view is one way to think about biology, one that
works especially well when we want to work out the logic of evolu-
tionary scenarios. It achieves this success by being agnostic about
many biological details, including what exactly a gene is or a how
development actually works. As a consequence, it loses potency in
situations where those details matter.
So far, the book has traced the origin and development of the
gene’s-eye view, clarified typical points of contention, and shown how
it helped us think about old evolutionary problems and pointed out
new ones. Biology has changed a lot in the half century since
Adaptation and Natural Selection and The Selfish Gene were written. In
these last few pages, I will look ahead and offer some reflections on
the standing of the gene’s-eye view and the nature of the field of
evolutionary biology.
Why should biologists study

the history of ideas?
A computational biology colleague of mine once described

evolutionary biology as a field obsessed with its own history. T hat
might well be true, but if so the obsession goes back a long way. Take,
for example, R.A. Fisher who wrote:
More attention to the History of Science is needed, as much by scien-
tists as by historians, and especially by biologists, and this should mean
a deliberate attempt to understand the thoughts of the great masters of
the past, to see in what circumstances or intellectual milieu their ideas
were formed, where they took the wrong turning or stopped short on
the right track. (Fisher 1959)
Scientists writing their own history is a double-edged sword. On the

one hand, they were there and therefore may know the ideas and people
involved. On the other hand, they were there, which means they have
vested interests in how these ideas and people fare when history is
182 conclusion: T h e ge n e’s-ey e v i ew today
written. Someone who was straddling that tricky balance was Ernst
Mayr, who has had an enormous influence on the way in which we
evolutionary biologists view our field, its history, and its philosophy.
Robert Trivers once described him as having ‘the strongest phenotype of
any organism [he had] ever met, man or beast’ (Trivers 2009) and books
like The Growth of Biological Thought (Mayr 1982), One Long Argument
(Mayr 1991), and This is Biology (Mayr 1998) have been read by many
aspiring evolutionary biologists. Readers of Mayr’s books, however,
receive one version of the history of biology. In particular, it quickly
becomes clear that the ideas that Mayr himself held dear (most notable
the biological species concept) fare rather well in his version of events.
This book is not a history book, but history plays an important role
and so does philosophy. I, like Mayr, am a biologist by training and
temperament, not a historian or a philosopher of science, and the
book should be read with that in mind.
Another issue with scientists writing their own history is the ques-
tion of who the intended audience is. Here, Mayr’s Harvard colleague
Stephen Jay Gould serves as a good example. Gould featured exten-
sively in some chapters of this book, as one of the most articulate and
public critics of the gene’s-eye view. In many ways, he filled the role
of critic-in-chief admirably (see, e.g., Dawkins’s tribute ‘Unfinished
correspondence with a Darwinian heavy weight’ published following
Gould’s death; Dawkins 2003, pp. 218–222). Gould was a fierce opponent
of what he considered the ‘hardening’ of the modern synthesis with
its increased focus on selection and gene-level explanations, as well as
a tireless advocate of hierarchy, constraints, punctuated rates of change,
and non-adaptive evolution (see, e.g., Gould 1980, 1983b; Brown 1999
and Sterelny 2007 provide readable overviews).
Gould often published his criticisms in popular magazines, rather
than scientific journals. Such public disagreements over the state of
contemporary evolutionary biology put his professional colleagues in
an awkward spot. For example, in his review of Daniel Dennett’s
Darwin’s Dangerous Idea (Dennett 1995)—a book that was very critical
of Gould—John Maynard Smith wrote:
Gould occupies a rather curious position, particularly on his side of

the Atlantic. Because of the excellence of his essays, he has come to be
seen by non-biologists as the preeminent evolutionary theorist. In
contrast, the evolutionary biologists with whom I have discussed his
work tend to see him as a man whose ideas are so confused as to be
hardly worth bothering with, but as one who should not be publicly
criticized because he is at least on our side against the creationists. All
this would not matter, were it not that he is giving non-biologists a
largely false picture of the state of evolutionary theory.
(Maynard Smith 1995).
Michael Ruse summarized Gould’s strategy as a ‘rather dangerous

game’ (Ruse 2013). In his attempt to be taken seriously by his colleagues
he was willing to air his grievances in public, in effect forcing
professional scientists to listen to him.
Dawkins also largely presented his arguments in public venues and
rejected the clear-cut separation between academic and popular writ-
ing. But if Gould sold radicalness, Williams and Dawkins offered
orthodoxy. This difference in approach is partly why I believe the
latter were more successful in their argument. I once got the advice
that if you want to change something within a conservative institution
(e.g. a university department), the best thing you can do is to present
your reform plan as the natural extension of the way things have
always been done. If you can successfully frame your proposal in such
a way, you can get away with really quite radical change.When Gould
put a lot of effort into presenting his ideas as novel and revolutionary—
his friend and colleague Richard Lewontin described him as being
‘preoccupied with the desire to be considered a very original and
great evolutionary theorist’ (quoted in Wilson 2015b)—Williams and
Dawkins would repeatedly tone down the radical nature of their
claims. In Adaptation and Natural Selection Williams noted that ‘genic
selection should be assumed to imply the current conception of
natural selection often termed neo-Darwinism’ (Williams 1966, p. 96)
and Dawkins insisted that the gene’s-eye view was simply the modern
expression of ‘orthodox neo-Darwinism’ (e.g. Dawkins 2013a, p. 264).
The gene’s-eye view was more radical than that. But through their
appeal to orthodoxy Williams and Dawkins were able introduce
comprehensive reform and dethrone the individual organism from
the centre of evolutionary explanations and install the gene in its
place.
Thinking about the role of individual scientists in history also
raises the question of what to do when our scientific heroes disap-
point us. I would not have written this book if I did not think
Dawkins had made a foundational contribution to our theoretical
understanding of evolution. On top of his technical work early in his
career, he spent most of his working life introducing evolutionary
biology to beginners, as a lecturer at the University of Oxford and to
a large global audience through his numerous best-selling books.
Lately, he has ruffled many feathers through his advocacy of atheism
and he has also been embroiled in various befuddling controversies
surrounding race and gender, typically originating on Twitter. In a
long, and overall very favourable, article in The Guardian titled ‘Is
Richard Dawkins destroying his reputation?’ his friend and intellec-
tual ally Daniel Dennett is quoted worrying that Dawkins was
‘seriously damaging his long-term legacy’ (Elmhirst 2015). I hope
Dawkins’s legacy will be the gene’s-eye view, but that is a subject for
future historians of biology.
For other thinkers featured in this book, it is possible to tell already.
I have extensively discussed the ideas of R.A. Fisher, including those
first put forward in papers like ‘Some hopes of a eugenicist’
(Fisher 1914). Recent years have seen increased scrutiny of Fisher’s
philosophical views, which have prompted several institutions to re-
evaluate their affiliation with him. In the span of a few weeks in the
spring of 2020, The Society for the Study of Evolution decided to
remove his name from the annual award given to the best paper
published by a graduate student in the journal Evolution and his former
Cambridge college debated taking down the stained window
commemorating him from its dining hall. Fisher’s scientific work
guarantees his place as one of the giants of modern biology. T

hat does
not mean that we need to celebrate him unquestionably.
Metaphors and mathematics
John Maynard Smith concluded his review of The Extended Phenotype

with the reflection that neither that book nor The Selfish Gene contains
a single line of mathematics. Yet, the logic was impeccable (Maynard
Smith 1982a). The same compliment can very much be paid to
Adaptation and Natural Selection: a deeply theoretical argument
expressed completely verbally and without equations.
The relationship between biology and mathematics has often been
rather awkward. T he lack of universal laws that could be captured
mathematically made the philosopher J.J.C. Smart deny that biology
counted as a proper science in his classic paper ‘Can biology be an
exact science?’ (Smart 1959; see Otsuka 2019). At the same time,
mathematics has long played an important role in evolutionary
biology. Population genetics has provided the formal backbone since
the 1930s, quantitative genetics allows selection to be measured in the
lab and in the field, and game theory unified the study of social
behaviour in microbes and humans.
The awkward relationship between the fields arises partly because
of the kind of mathematical models used in biology. As J.B.S. Haldane
put it in his reply to Ernst Mayr beanbag genetics criticism: ‘Our
mathematics may impress zoologists but do not greatly impress math-
ematicians’ (Haldane 1964). T oday the situation is very different. Even
if one does not want to go so far as Markowetz (2017) and claim that
‘all biology is computational biology’, a casual browsing through the
major journals in the field reveal that biology can hold its own when
it comes to mathematical sophistication. Mathematical models are
now an indispensable tool in evolutionary biology (Nowak 2006;
Hartl and Clark 2006; Otto and Day 2007). T hese models come in a
variety of shapes and forms. They may involve formal analytical

methods, providing exact solutions to different population genetic
scenarios. They may be statistical in nature, capturing variances and
co-variances of biological traits and fitness. And, when things get
really messy, these techniques can be incorporated into computer
simulations allowing even more complex problems to be solved.
Together, quantitative approaches help us sharpen our intuitions,
uncover hidden assumptions, and develop predictions that can be
tested empirically.
But there is more to theory in evolutionary biology than math
ematical models (Pigliucci 2013; Otsuka 2019). The history of the
gene’s-eye view show that verbal-conceptual models are not just a
second rate alternative to mathematic models, but the two often
actively work in tandem (Servedio et al. 2014;Yanai and Lercher 2020).
Verbal-conceptual models often lead the way to new areas that can
then be captured in a more formal way.
At the core of many verbal-conceptual models are metaphors. This
is true of The Selfish Gene, as well as The Origin of Species (less so
Adaptation and Natural Selection). Metaphors are more than simple ver-
bal descriptions (Olson et al. 2019 and Kampourakis 2020). T heir
expressiveness triggers our imagination and stimulates our thinking;
they let us see connections that otherwise would have remained
obscure. Furthermore, the fact that many metaphors are rather vague
is not necessarily the disadvantage it is often portrayed to be but,
instead, it allows diverse biological phenomena to be brought together.
Like with anthropomorphizing, the use of metaphors tend to make
certain scientists uncomfortable (see, e.g., Pauwels 2013). As the
pioneering cyberneticists Arturo Rosenblueth and Norbert Wiener
warned: ‘the price of metaphor is eternal vigilance’ (quoted in
Lewontin 2001). Good scientific metaphors persist because they help
make sense of the world; they make us ask the right questions that can
be answered empirically. T he best metaphors, like good mathematical
models, highlight certain aspects of a biological phenomenon. The
flip side is that it ignores other aspects. For instance, the idea of the
‘tree of life’ beautifully captures the idea of common ancestry and

degrees of relatedness. It may also make us resist evidence of hybridi-
zation, horizontal gene transfer, and endosymbiosis. T hinking about
the evolutionary fate of competing individual genes is a forceful way
to sort out the logic of different selective scenarios and the gene’s-eye
view effortlessly highlights the potential for genomic conflicts. It can
also obstruct our focus on genetic drift and developmental constraints.
Rosenblueth and Wiener’s call for vigilance reminds us that we should
always worry not only about what questions a metaphor makes us ask,
but also what questions that go unasked.
Alfred Russel Wallace was very concerned with the phrase ‘natural
selection’, which he thought implied a selector. In a 1866 letter, he
even tried to convince Darwin to abandon the term in favour of
Herbert Spencer’s ‘survival of the fittest’ (Darwin Correspondence
Project 2020e). In response, Darwin argued that the worries about the
metaphor of natural selection would go away by acquiring ‘a little
familiarity’ with it (Darwin 1868, p. 6). As I set out in the Introduction,
I believe the same can be achieved with the gene’s-eye view. A little
bit of familiarity may also help avoid the issue known as reification.
This fallacy occurs when metaphors or abstract constructions are
treated as if they were real physical things: ‘a map is not the territory’
as Korzybski (1933, p. 58) put it. Throughout this book, I have
described several instances where critics of the gene’s-eye commit this
fallacy. At the same time, I have noted how proponents of the perspec-
tive, most notably Dawkins, must share some of the blame for this by
conflating genic selection as a process and as a perspective.
In general, biology will suffer if there is too much focus on abstract
principles. This was the worry of Dawkins’s doctoral advisor Niko
Tinbergen who late in his career commented on the modern study of
behaviour:
The more abstract thinking of Maynard Smith, Hamilton, Trivers, and
Dawkins I do not completely understand, and moreover, I suspect that
they know too few animals, and know too little about the multitude
of phenomena and aspects. (Tinbergen 1980, quoted in Kruuk 2003)
Biologists should never lose sight of animals (or other kinds of organ-
isms, from Archaea to orchids). The gene’s-eye view is not the only
way to think about evolution and natural selection, and for some
questions it is not the best. But the odds of getting the most out of it
will increase if one understands what biological aspects it tends to
favour and why.
Die, selfish gene, die?
Throughout this book I have documented several instances where the

gene’s-eye view has stirred up strong emotions among biologists,
philosophers, and laypeople. Such incidents are not just something of
the past, but selfish genes are routinely used as the starting point by
writers who want to pontificate about what is wrong with
contemporary evolutionary theory. For example, in the fall of 2020, a
special issue in New Scientist on ‘the changing face of our greatest
theory of nature’ came with the splash ‘Move over, selfish gene’
(Barras 2020). In December 2013, the journalist David Dobbs applied
a similar rhetorical approach in his long essay in Aeon, a digital
magazine, titled ‘Die, selfish gene, die’ (Dobbs 2013). The gist of
Dobbs’s criticism was that new discoveries in gene regulation and
developmental biology undermines the picture of evolution painted
by the gene’s-eye view. Dobbs succeeded in causing a stir and even
got Dawkins to publish a reply on his foundation’s website
(Dawkins 2013b).
The criticism that evolutionary theory is failing to properly
incorporate certain biological phenomena is not new (Welch 2017).
Often, the complaint takes the form of lists of ‘things in biology that
interests me’ (to paraphrase Clement Attlee’s jibe against Winston
Churchill’s books on English history). Items on the lists may or may
not have much to do with each other, and the same items may or may
not appear on different lists. Other than developmental biology, things
that often make an appearance on the list of what’s wrong with
evolutionary biology are phenotypic plasticity (Pigliucci 2001; West-

Eberhard 2003), niche construction (Odling-Smee et al. 2003), and
evolvability (Wagner 2005; ironically, Dawkins was one of the first to
write about the ‘evolution of evolvability’ in Dawkins 1988).
There is an ongoing polemic whether these diverse observations
demand an extended evolutionary synthesis (Pigliucci and Müller
2010; Laland et al. 2014, 2015; Charlesworth et al. 2017; Futuyma 2017;
Huneman and Walsh 2017).What is at stake, and what according to its
proponents needs an extension, is the modern synthesis of the 1930s
and 1940s. The modern synthesis means different things to different
people, and as a consequence critics have focused on different aspects,
ranging from empirical to historical and philosophical ones (Gayon
and Huneman 2019; Lewens 2019b). In an attempt to capture the
essence of the modern synthesis, Huneman (2017) quotes Julian
Huxley, a chief architect who coined the term in his book, the massive
Evolution: The Modern Synthesis (Huxley 1942). In a letter to Ernst
Mayr, Huxley described it as:‘Natural selection, acting on the heritable
variation provided by the mutations and recombination of a Mendelian
genetic constitution, is the main agency of biological evolution’
(Huxley 1951, quoted in Huneman 2017, p. 71). The modern synthesis
was more than the emergence of population genetics; it also included
ecology, systematics, cytology, and palaeontology. Nevertheless,
Huneman describes gene-centrism and adaptationism as the ‘heart
and soul’ of the modern synthesis. This combination sounds very
much like the gene’s-eye view. T hat being said, biologists have long
differed in whether they accept the whole package, and there are
prominent examples of biologists accepting one but not the other. For
example, Mayr endorsed natural selection as the main agent of evolu-
tion but rejected gene-centrism (Mayr 1959, 1983). At the opposite
end, Michael Lynch strongly favours focusing on genes, writing that
‘nothing in evolution makes sense except in light of population genet-
ics’, while also describing what he calls the ‘Dawkins agenda to spread
the word on the awesome power of natural selection’ as ‘misleading’
(Lynch 2007b).
As noted above, both Williams and Dawkins considered their views

to be capturing the insights of the modern synthesis. Regardless
whether the modern synthesis at its core boils down to gene-centrism
and adaptationism or not, recent and past debates suggest that there is
more to the call for an extended evolutionary synthesis than just
scientific disagreements over models and data. It also reflects a deeper
division over how evolution should be construed. Take, for example,
Sean Carroll, the eloquent spokesperson for evolutionary develop
mental biology and critic of the gene’s-eye view who wrote:
Millions of biology students have been taught the view (from popula-
tion genetics) that ‘evolution is change in gene frequencies.’ (…) This
view forces the explanation toward mathematics and abstract descrip-
tions of genes, and away from butterflies and zebras (…) The evolution
of form is the main drama of life’s story, both as found in the fossil
record and in the diversity of living species. So, let’s teach that story.
(Carroll 2005, p. 294)
I personally find the story told by the gene’s-eye view both dramatic
and inspiring. It is my experience, however, that whether this picture
is shared by others depend both on what biological questions that
they are interested in, and how the gene’s-eye view fits into the
general intellectual environment where they received their scientific
or philosophical training.
The gene’s-eye view worldwide
Kim Sterelny once divided up evolutionary biology into what he

called an American and a British tendency (Sterelny 2001, pp. 4–5).
These two tendencies differ in their attitudes towards a number of
issues. The British tendency has emphasized adaptation as the central
problem of evolutionary biology, whereas the American has focused
on diversity and its constraints. Following from this, the British
tendency has given more weight to selective explanations, whereas
the American has highlighted the importance of historical and chance
explanations. This division is, of course, built on exaggeration and

overgeneralization. For example, George Williams and Daniel Dennett,
both Americans, would make great representatives of the British
tendency. Nevertheless, in Chapter 1 I argued that the gene’s-eye view
grew out of a distinctly British intellectual environment. Anecdotally,
its influence across the world appears to be heterogeneous.
Karl Popper aptly described science as ‘knowledge without a
knower’ (Popper 1972, p. 109). The universe is out there and its
properties does not change depending whether members of Homo
sapiens can correctly describe them or not. From such a commitment
to realism does not necessarily follow that there is only one way to
describe those properties. Scientific theories are human constructs,
which means one can ask questions about their origin and subsequent
spread. For example, to what extent is the theory of evolution by
natural selection a product of Darwin’s quintessential British upper
middle class upbringing? In a rather unusual book, two Darwin
scholars, Robert Richards and Michael Ruse, debate this question
(Richards and Ruse 2016). To Ruse, himself a Brit, the defining fea-
tures that led to Darwin’s theory were British in nature: the industrial
revolution, notions of social progress, the Anglican Church, and
thinkers like Robert Malthus, Adam Smith, and William Paley. In
contrast, Richards paints the picture of a much more cosmopolitan
Darwin: one deeply influenced by French, and especially German
contemporaries. Richards argues that rather than British Enlightenment
figures, no other thinker had a stronger influence on the young
Darwin than Alexander von Humboldt.
If Richards and Ruse deal with the origin of Darwin’s theory, there
is also a steady increase in the interest in so-called ‘reception studies’.
This research centres on how the theory of evolution was received in
different countries, typically outside the European and American
context. Examples in the genre include China and Charles Darwin
(Pusey 1983), From Man to Ape: Darwinism in Argentina, 1870–1920
(Novoa and Levine 2010), and Darwin, Dharma, and the Divine:
Evolutionary Theory and Religion in Modern Japan (Godart 2017). To my
knowledge, there have been no corresponding studies of the spread of

the gene’s-eye view.
One exception is Osamu Sakura’s analysis of the reception of
sociobiology in Japan (Sakura 1998). To many evolutionary biolo-
gists, Japan is primarily known for being the home of Motoo
Kimura, who developed the neutral theory of molecular evolution
(Kimura 1968). Much debated ever since its conception, neutral
theory stimulated plenty of work and led to many theoretical and
empirical advances (see Kern and Hahn 2018 and Jensen et al. 2019
for two contrasting takes on its current standing). As Sakura shows,
however, Japanese evolutionary biology in the post World War II era,
was influenced as least as much by the ecologist Kinji Imanishi, who
was strongly critical of Darwin. Publishing almost exclusively in
Japanese, and with great popular success, Imanishi rejected the idea
that competition within and between species played any significant
role in evolution and instead emphasized an inherent harmony in
the living world (Halstead 1985).After the dominance of the Imanishi
school, the arrival of sociobiology was a breath of fresh air. The
Selfish Gene and The Extended Phenotype were both translated to
Japanese, and so were On Human Nature (Wilson 1978) and Evolution
and the Theory of Games (Maynard Smith 1982b). The younger gen-
eration of Japanese (evolutionary) ecologists rapidly incorporated
these ideas.
I have discussed the reception and standing of the gene’s-eye view
with colleagues from various countries in Europe, South America,
and Asia. These conversations suggest that the specific sub-field within
evolutionary biology that has been dominant in a country matters for
the standing of the gene’s-eye view. Maynard Smith once remarked
that he ‘never knew a birdwatcher who was not a naive adaptationist’
(Kohn 2004, p. 6). Countries where behavioural ecology has been
strong also seemed to have embraced the gene’s-eye view faster. This
includes my native Sweden where bird- watching behavioural
ecologists were instrumental not only in the professional organization
of the field, such as the founding of the Evolutionary Biology Centre
at Uppsala University, but also in the popularization of evolution (see,

e.g., Ulfstrand 2008).
Evolutionary biology is a small field, which means that a few deter-
mined individuals may be able to leave an especially long-lasting leg-
acy. Sakura (1998), for example, stress the importance of the ‘three
musketeers’ of Japanese sociobiology, Toshitaka Hidaka, Yoshiaki Itô,
and Yûji Kishi for organizing translations of key books and for pushing
the field forward. At this stage, these inferences from Sweden and
Japan are all anecdotal but highlight the need for systematic culturally
comparative reception studies.
Final thoughts
Throughout this book I have tried to guide the reader through the
many-times quite intricate and sprawling literature that surrounds the
gene’s-eye view. Regardless of whether we consider it a Pareto error
or the primus inter pares of all ways to think about evolution, I believe
that by understanding its origin, logic, and implications will help us
realize its full potential.
I have often been frustrated by debates over the value of the gene’s-
eye view, both among scientific colleagues and in the public arena,
and equally so by its supporters and its critics. It is my hope that this
book can contribute some nuance to this discourse and that, after
having made it this far, the reader will leave with a little bit familiarity
with this special way to read nature.
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Wynne-Edwards VC. 1963. Intergroup selection in the evolution of social
systems. Nature. 200: 623–626.
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Yanai I and M Lercher. 2020. The two languages of science. Genome Biology.
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Zuk M. WD Hamilton. Science. 218: 384–387.
Zurita S, Cabrero J, López-León MD, and JPM Camacho. 1998. Polymorphism
regeneration for a neutralized selfish B chromosome. Evolution. 52: 274–277.
OUP UNCORRECTED AUTOPAGE PROOFS – <STAGE>, 28/05/21, SPi
Index
Tables and boxes are indicated by an italic t and b following the page number.
acquired characteristics, inheritance B chromosomes 165, 169–70, 172, 174
of 62 ‘balance of nature’ concept 21
action at a distance 156–7 Barash, David P. 44–5
active germ-line replicators 62 Barkow, Jereme 177
Adaptation and Natural Selection Barlow, Nora 21
(Williams) 2, 12, 24, 38–40, 41–2, Bateson, Patrick 103–6
44, 46–9, 51, 90, 99, 129–30, 175, Bateson–Dobzhansky–Muller
183, 185 incompatibilities 173
adaptationism 12–25, 137–43, 176 Batty, Charles 139
Aeon 188 beanbag genetics 25–6, 185
agential thinking 57, 86–8, 103–4 beaver dams 155
Aiken, George 100 behavioural ecology 87, 192–3
Akçay, Erol 144–6, 149 beneficiary of selection question 4–5,
Allee, W.C. 37–8, 39 60, 61–2, 76, 77, 78, 101
Allen, Benjamin 133, 138 Bentley, Michael 40
altruism 36, 43, 80 Biernaskie, Jay M. 162
see also inclusive fitness and biological hierarchy 35–6, 72–8, 98–9, 176
Hamilton’s Rule; kin selection biology
American Naturalist 47, 120–1, 132, 174 philosophy of 6, 47–8, 54–5
American Society of Naturalists 50 uniqueness of 85–6
Ancestor’s Tale,The (Dawkins) 58 Biology and Philosophy 137, 154, 156
Anglican Church 14, 15, 17, 191 Bioscience 47, 132
animal architecture 155–6 Blackmore, Susan 66
Animal Dispersion in Relation to Social blending inheritance 71, 135
Behaviour (Wynne-Edwards) 37–8, Blind Watchmaker,The (Dawkins) 23, 63
40 Bonner, John Tyler 74
Ant and the Peacock,The (Cronin) 80–1 bookkeeping objection 82, 97–103
anthropomorphism 81, 82–9, 103–4 Bourke, Andrew 78, 143
licensed 89 Boyle Lectures 15
ants Brandon, Robert 48, 59
carpenter 158 Bridgewater Treatises 18
red fire 161, 163 Brief Candle in the Dark (Dawkins) 132
Ardrey, Robert 40 Briggs, Andrew 113
armpit effect 160 brood parasitism 157
atheism 14, 15, 17, 18, 22–3, 184 Burt, Austin 167, 174
averaging fallacy 94–6 Buss, Leo 72, 74, 76
236 I n de x
Cain, Arthur 22 A Devil’s Chaplain 111

Camponotus castaneus 158 expanded definition of
cancer 62 environment 34–5
Carroll, Sean 18, 190 The Extended Phenotype 59, 76,
causality 82, 97–103 99–100, 104, 132, 151–2, 153–4, 155,
Charkin, Richard 46 159, 185
Charlesworth, Brian 104 extended phenotypes 75, 153–9
Comfort, Nathaniel 3 Gaia hypothesis and 111–12
continuity of the germ-plasm 62 genes as information 64
contrivance 16, 17–18, 20, 140 genes as types 56
Conway Morris, Simon 3 gene’s-eye view as process or
Cosmides, Leda 167, 175, 176–7 perspective 68–9, 100, 187
Crafoord Prize in Biological genetic determinism 104
Sciences 39 greenbeards 159–64
Crick, Francis 85, 166 group selection 13, 40, 76–7, 132–3
CRISPR-Cas9 technology 170 Hamilton’s work 116–18, 139
criticisms of gene’s-eye view 2–6, human nature and morality 109,
80–115, 188–90 110–11, 114
anthropomorphism 81, 82–9, 103–4 inclusive fitness 129, 130, 131–4
bookkeeping objection 82, 97–103 intentional language 81, 83, 88
genetic determinism 82, 103–8, interactions between genes 81–2,
109–10 89–91, 93–4
human nature and morality 82, length of genes 53
108–15 memes 49, 65, 67
interactions between genes 81–2, Necker cube illusion 99–100, 101
89–97, 95t neo-Paleyan biology 20, 21–3
Cronin, Helena 80–1 origin of ‘selfish gene’ concept 44
Cuckoo, European 157 paradox of the organism 75
cultural evolution 64–8 parasites 75, 154, 157–8
Cunningham, Conor 59 religion 66
cytoplasmic male sterility 165, 168 replicators and vehicles 57–8, 59,
61–2, 63, 64, 68, 71, 100–1
Darwin, Charles 1–2, 6, 14, 19–20, 24, responses to criticisms 83, 88, 94,
25, 36, 64, 69, 86, 87, 108–9, 111, 105, 109
180, 187, 191 River Out of Eden 111
Darwinian Populations 70 rowing analogy 35, 81–2, 89–91, 93
Davies, Nicholas B. 143 selfish genetic elements 141, 165–6,
Davin, Dan 12 175
Dawkins, Richard 2, 4, 18, 43–4, selfish nucleotide theory 54
153, 180 sociobiology 110
adaptationism 20, 21–3 Unweaving the Rainbow 34–5, 93, 111
agential thinking 57, 88 see also Selfish Gene,The
The Ancestor’s Tale 58 Dennett, Daniel 48, 66, 80–1, 152, 182,
appeal to orthodoxy 183–4, 190 184, 191
atheism 22–3, 184 Descartes, René 85
biological hierarchy 75–7 design, appearance of 12–25, 87, 119,
The Blind Watchmaker 23, 63 137–43
Brief Candle in the Dark 132 determinism, genetic 82, 103–8, 109–10
definition of gene 48–9, 51, 94 developmental biology 103–8
I n de x 237
developmental systems theory 82, Fisher Box, Joan 27

106–8 FLO1 gene 162–3
Devil’s Chaplain, A (Dawkins) 111 flocculation 162–3
Dialogues Concerning Natural Religion Ford, E.B. 22
(Hume) 22–3 Formal Darwinism Project 24, 119,
Dictyostelium discoideum 163 137–43
DNA Franklin, Rosalind 85
genome size 166 Frisch, Karl von 155
non-coding 166 Fromhage, Lutz 146–9
see also genes; selfish genetic elements Fundamental Theorem of Natural
Dobbs, David 188 Selection 30–5, 32b
dominance 26, 29, 34, 92
Doolittle, Ford 166 Gaia hypothesis 111–12
Dover, Gabby 74–5 game theory 43, 76, 185
Drosophila 164–5, 169, 171, 173 Gardner, Andy 3, 16, 23–4, 56, 57, 71,
124, 135, 137, 139–40
Eberhard, W.G. 175 gene drives 170
Edwards, A.W.F. 27, 28, 31 genes
Eigen, Manfred 71 agential thinking 88
Eldredge, Niles 75–6, 118 average effect 89–91
Elliott, Roger 11 as beneficiaries of natural
Emerson, A.E. 39, 40 selection 4–5, 61–2, 77, 78, 101
environment, expanded definition definitions 48–53, 94
of 29, 33–5, 52–3, 90, 97, 136 gene-P and gene-D 51–2
epigenetics 52, 105 as information 63–4, 107
epistasis 26, 28, 34, 91–4 length of 53–5
Evolution 39, 92–3, 184 parliament of 147–8
‘The evolution of eusociality’ (Nowak, reference genes 148
Tarnita, and Wilson) 123–4, 132–3, replicator concept 48–9, 57–64, 68,
134 70–2, 100–1
Evolution of Individuality,The (Buss) 74 strategic genes 56
evolutionary developmental biology as types or tokens 55–7, 63
(evo-devo) 106 genetic determinism 82, 103–8, 109–10
evolutionary medicine 39 genetic drift 52, 91, 136
evolutionary psychology 176–7 ‘genetic program’ metaphor 104
evolvability 189 genetic variance, Fisher’s definition
extended evolutionary synthesis 189, of 28, 31, 32b
190 Genetical Theory of Natural Selection,The
Extended Phenotype,The (Dawkins) 59, (Fisher) 29–30, 31, 92, 120
76, 99–100, 104, 132, 151–2, 153–4, genic pluralism 101–3
155, 159, 185 genome size 166
extended phenotypes 75, 152, 153–9 genomic conflicts
eye, human 18, 19, 24 adaptation and 140–2
greenbeards 161–2
Felsenstein, Joe 97 inclusive fitness and 140–2, 149
Feynman, Richard 7 mitochondrial versus nuclear
Fisher, R.A. 12, 13, 20–1, 25, 26–35, 32b, genes 141–2, 165, 167–8, 175
37, 43, 51, 52–3, 90, 92–3, 98, 107–8, sex ratios and 130–1, 165
120, 130–1, 136, 181, 184–5 see also selfish genetic elements
238 I n de x
genomic cooperation 93, 178 homing endonucleases 170

Gershenson, Sergey 164–5 Hooker, Joseph Dalton 108–9, 111
Ghiselin, Michael 59 Hudson, Colin 120
Gifford Lectures 18 Hughes, David 154
Godfrey-Smith, Peter 70, 84 Hull, David 57, 58, 59–60, 68
Gould, Stephen Jay 2, 19, 22, 47, 59, human eye 18, 19, 24
70–1, 75, 76–7, 80–1, 82, 94, human nature and morality 82,
97–100, 175–7, 180–1, 182–3 108–15
Gould’s paradox 70–1 Humboldt, Alexander von 191
Gp-9 greenbeard gene 161, 163 Hume, David 16, 22–3, 114
Grafen, Alan 23–4, 27, 31, 89, 119, Huneman, Philippe 189
137–9, 141, 161–2 Hurst, Greg 171
Graff, Gerald 7 Huxley, Julian 29, 38, 189
Gray, Asa 20 Huxley, T.H. 20, 112–13, 164
Gray, John 66 hybridization 172–3
greenbeards 152, 159–64
Griffiths, Paul E. 107 Imanishi, Kinji 192
group selection 13, 35–43, 76–7, 96, 100, immortality of replicators 61–4
132–3, 175 inclusive fitness and Hamilton’s
see also multilevel selection models Rule 13, 40–1, 116–50
Guardian,The 134, 184 appearance of design and 87, 119,
137–43
Hacking, Ian 48 controversy about 123–9
Haig, David 49–50, 56, 57, 108, 142, 160 folk definition of inclusive
Haldane, J.B.S. 13, 25–6, 37, 165, 185 fitness 146–9
Halvorson, Hans 113 Formal Darwinism Project 24, 119,
Hamilton, W.D. 2, 4, 12, 13, 40–1, 47, 71, 137–43
116–18, 120, 123, 130–1, 140, 144, gene tokens and 56–7
159, 174 general version of Hamilton’s
Hamilton’s Rule see inclusive fitness and Rule 124–9, 125b, 135–6, 140
Hamilton’s Rule gene’s-eye view and 119, 121–2,
Hanke, David 84 129–37, 130t, 143–9
Hansell, Mike 156 genetic lineage view of inclusive
Hardy, G.H. 27 fitness 144–6, 149
Harvey, P. 117 Hamilton’s definition of inclusive
haystack model of group selection 41 fitness 122–3
Heath, Edward 11 major transitions and 77, 78
heredity see inheritance origin of 120–3
heterozygous advantage 29, 94–7, 95t, 141 phenotypic gambit 141
Hidaka, Toshitaka 193 individuality, transitions in 72, 73–4
hierarchical organization of life 35–6, see also major transitions
72–8, 98–9, 176 information, genes as 63–4, 107
Hinde, Robert 105–6 inheritance
historical origins of gene’s-eye view 2, of acquired characteristics 62
11–45 blending 71, 135
adaptationism and natural particulate/Mendelian 13, 25, 27–8,
theology 12–25 30, 50, 51, 67, 71, 94, 135
group selection 13, 35–43 intelligent design 7, 55, 66
origin of term 44–5 intentional language 81, 82–9, 103–4
population genetics 13, 25–35 interactors 57, 59–60, 76, 99, 101
I n de x 239
International Society of Behavioural MacArthur, Robert 80

Ecology 132–3 McClintock, Barbara 165
invasion fitness 144–6 McGrath, Alister 18, 19
Itô,Yoshiaki 193 Mackie, John 83
Madgwick, P.G. 160
Jacob, François 104 major transitions 72–8, 142–3
James, William 64 transitions in individuality 72,
Japan 192, 193 73–4
Jennions, Michael 146–9 Major Transitions in Evolution,The
Johannsen, Wilhelm 50, 52 (Maynard Smith and
Journal of Genetics,The 156 Szathmáry) 72–5, 142
Journal of Theoretical Biology,The 122 Mallett, Jim 117
Malthus, Robert 191
Kant, Immanuel 14–15, 16, 86 Maschler, Tom 61
Karlin, Sam 30 mathematical models 185–6
Kimura, Motoo 192 Maynard Smith, John 2, 12, 21, 22, 37,
kin selection 37, 40–1, 71, 118, 123, 129, 39, 41, 43, 70, 72–5, 76, 80–1, 88, 94,
135, 162 102–3, 109–10, 121, 123, 131–2, 142,
Kishi,Yûji 193 182–3, 185, 192
Kitcher, Philip 51, 101 Mayr, Ernst 6, 19–20, 25–6, 39, 66, 92,
Kohn, Marek 22 93, 104, 182, 185, 189
Krebs, John R. 143, 156–7 Medawar, Peter 93
Kropotkin, Peter 113 meiosis 53–4, 67, 147–8, 169
Kuhn, Thomas 47–8 memeplexes 65
memes 49, 64–8
Lack, David 38 Mendel, Gregor 25, 50, 51
Lamarckian inheritance 62 Mendelian inheritance 13, 25, 27–8, 30,
Langley, Charles 47 50, 51, 67, 71, 94, 135
Laplace, Pierre-Simon 16 metaphors 186–7
Leber’s hereditary optic mice 156, 169, 175
neuropathy 168–9 Midgley, Mary 82–3, 104, 112
Leigh, Egbert 147, 175 mitochondrial genomes 53, 55–6,
levels of selection debate 13, 35–43, 141–2, 165, 167–9, 175
72–8, 96, 98–9, 100, 132–3, 176 modern synthesis 189–90
Levins, Richard 80, 155 see also population genetics
Lewens, Tim 18, 23 Monod, Jacques 1, 104
Lewontin, Richard 2, 22, 29, 43, 46, 47, Moore, G.E. 114
69–70, 80, 91, 94–6, 95t, 98, 109, morality and human nature 82,
131, 155, 174, 175, 183 108–15
Lewontin’s Principles 69–70 Morgan, Thomas Hunt 50, 51
licensed anthropomorphism 89 Moss, Lenny 51–2
linkage disequilibrium 53–4 Mother’s Curse 168–9
Literary Churchman 20 moths
Lloyd, Elisabeth 48, 60, 77, 101, European gypsy 158
102, 142 peppered 171
Lloyd’s four questions 60 Muller’s ratchet 172
logical vs. literal thinking 5–6 multilevel selection models 74, 77
Lorenz, Konrad 40, 155 see also group selection; levels of
Lubbock, John 19 selection debate
Lynch, Michael 189 Murdoch, Iris 6
240 I n de x
Nabi, Isadore 80 gene’s-eye view’s concept of 158

natural selection paradox of the organism 75
abstract formulations of 68–78 uniqueness of 85–6
beneficiary question 4–5, 60, 61–2, see also biological hierarchy; inclusive
76, 77, 78, 101 fitness and Hamilton’s Rule;
Darwin 1–2, 6, 20, 24, 25, 69, 86, replicators and vehicles
87, 187 Orgel, Leslie 166
Fisher’s Fundamental Theorem 30–5, Östergren, Gunnar 165, 174
32b Oxford Surveys in Evolutionary Biology 75
group selection 13, 35–43, 76–7, 96, Oyama, Susan 107
100, 132–3, 175
levels of selection debate 13, 35–43, P element 173
72–8, 96, 98–9, 100, 132–3, 176 Paley, William 13, 15–25, 191
pluralistic gene selectionism 101–3 paradox of the organism 75
recipe approach 69–70 parasites 75, 154, 157–8
replicator–vehicle approach 48–9, parent–offspring conflict 43
57–64, 68, 70–2, 100–1 Pareto,Vilfredo 180
Natural Selection: Domains, Levels and Pareto errors 180–1
Challenges (Williams) 24, 64, 99 Parker, Geoffrey 42–3
natural theology 13–25 parliament of genes 147–8
Natural Theology (Paley) 13, 15–18, 19, parsimony 13, 42
20, 21, 24 Patten, Manus 89
Nature 2, 3, 41, 43, 47, 74–5, 80, 109, Pearson, Karl 27, 50
123–4, 131, 132–3, 166 phenotypes 50, 51–2, 53, 69
nature versus nurture dichotomy 107–8 see also extended phenotypes
Necker cube illusion 99–100, 101 phenotypic gambit 141
neo-Paleyan biology 18–25, 119, 137–43 phenotypic plasticity 189
Nesse, Randolph 39, 88, 110–11 philosophy of biology 6, 47–8, 54–5
neutral theory of molecular Pinker, Steven 18, 133
evolution 192 Plantinga, Alvin 18
New Scientist 110, 132, 188 pluralistic gene selectionism 101–3
New York Review of Books,The 2–3, 80–1, Popper, Karl 47–8, 191
93, 176–7 population genetics 13, 25–35, 51, 137, 185
New York Times,The 47 Powell, Baden 14
Newtonian physics 15, 17, 128 Price, George 30, 31–3, 35, 43
niche construction 155–6, 189 Price equation 125b, 135, 136
Nieuwentyt, Barnard 16 Provine, William 25, 26
Noble, Denis 5, 6, 72 punctuated equilibria 75
non-additive genetic effects 32b, 34, Punnett, R.C. 27
35, 90
see also dominance; epistasis Quarterly Review of Biology,The 46–7
non-coding DNA 166 Queller, David 124, 125b, 136
Nowak, Martin 123–4, 132–3, 134–5, 138 Quinton, Anthony 12
Odling-Smee, John 155 realism, tempered 101–3

Okasha, Samir 32b, 70–1, 76, 87 reception studies 191–2
Ophiocordyceps unilateralis 158 recombination 53–4
optimization theory 56 reductionism 54–5
organisms 1–2, 3, 4–5 reference genes 148
agential thinking 87 reification 187
I n de x 241
replicators and vehicles 48–9, 57–64, rowing analogy 35, 81–2, 89–91, 93
68, 70–2, 100–1 title of 61, 93
restorer genes 168 selfish genes
retrotransposons 170–1 as beneficiaries of natural
Richards, Robert 191 selection 4–5, 61–2, 77, 78, 101
Ridley, Mark 75, 113, 161–2 definitions 48–53, 94
Ridley, Matt 3 as information 63–4, 107
River Out of Eden (Dawkins) 111 length of 53–5
RNA replicator concept 48–9, 57–64, 68,
genomic cooperation 178 70–2, 100–1
retrotransposons 170–1 as types or tokens 55–7, 63
Rodgers, Michael 11–12, 46, 58, 93 selfish genetic elements 124, 140–2,
Rose, Steven 109–10 152–3, 164–78
Rosenberg, Alex 54–5, 84 B chromosomes 165, 169–70, 172, 174
Rosenblueth, Arturo 186 co-evolution with suppressors 173
Roughgarden, Joan 114 early work on 164–7
rowing analogy 35, 81–2, 89–91, 93 gene’s-eye view and 174–8
Royal Society of Edinburgh 27, 29 homing endonucleases 170
Royal Society of London 3, 22, 27 hybridization and 172–3
Royal Swedish Academy of importance of sex for 171–2
Sciences 39 meiosis and 169
Ruse, Michael 6, 18, 20, 183, 191 mitochondrial genomes 141–2, 165,
Russian doll analogy 77–8 167–9, 175
restorer genes 168
Saccharomyces sp. 162–3 segregation distorters 126, 140, 169
Sagan, Carl 18 sperm killers 169
Sahlins, Marshall 109, 118 suppressors 173
Sakura, Osamu 192, 193 t-haplotype of mice 169, 175
Sapienza, Carmen 166 transposable elements 165, 166,
Schrödinger, Erwin 85 170–1, 172, 173
Science 46, 47, 130–1 selfish nucleotide theory 54–5
Scott, Thomas W. 177–8 sex ratios 130–1, 165
Scruton, Roger 3 sexual selection 80, 114
Seger, J. 117 shifting balance theory 37
Segerstrale, Ullica 5–6, 91, 110, 174 sickle-cell anaemia 95
selection coefficients 94–6, 95t Simpsons, George Gaylord 109
Selfish Gene,The (Dawkins) 2, 3, 4, 5, 44, Skilling, Jeffrey 3
185, 186 Slatkin, Montgomery 54
criticisms of 47, 82–3, 103, 104–5 Slobodkin, Lawrence 46–7
definition of gene 48–9, 51 Smart, J.J.C. 185
expanded definition of Smith, Adam 191
environment 34, 35 Sober, Elliot 29, 48, 60–1, 76, 94–6, 95t,
greenbeards 159 98, 102
group selection 76 social behaviours
Hamilton’s work 116–18 greenbeards and 152, 159–64
human nature and morality 109, group selection and 13, 35–43
110–11, 114 kin selection 37, 40–1, 71, 118, 123,
philosophy of biology and 47–8 129, 135, 162
publication of 11–12, 46 see also inclusive fitness and
replicators and vehicles 57–8, 59, 61 Hamilton’s Rule
242 I n de x
social media 49, 65 Wade, Michael 35, 36, 94

sociobiology 43, 80, 109, 110, 111, 192, 193 Wallace, Alfred Russel 187
Sociobiology (Wilson) 37, 43, 80, 117, 132 watch analogy 16
Solenopsis invicta 161, 163 Waters, Kenneth 101, 102
Spandrels of San Marco 22, 47 Watson, James 85
Spencer, Herbert 64, 112, 187 Weber, J.N. 156
sperm killers 169 Weinberg, Steven 128
Stamp Dawkins, Marian 180 Weismann, August 62
Steane, Andrew 113 Werren, Jack 167, 171
Stearns, Stephen 97 Wiener, Norbert 186
Stebbins, G. Ledyard 39 Wilkins, Maurice 85
Stent, Gunther 50 Williams, Doris 40, 129
Sterelny, Kim 6, 51, 101, 107, 108, 190 Williams, George C. 2, 38–9, 191
strategic genes 56 adaptation 24, 41–2
Structure of Evolutionary Theory,The Adaptation and Natural Selection 2, 12,
(Gould) 97–8, 175 24, 39–40, 41–2, 44, 46–9, 51, 90,
Sturtevant, Alfred 51 99, 129–30, 175, 183, 185
Sullivan, Lucy 84, 88 appeal to orthodoxy 183–4, 190
suppressors biological hierarchy 77
of greenbeards 161–2 causality 99
of selfish genetic elements 173 definition of gene 48–9, 51
see also restorer genes expanded definition of
Sweden 192–3 environment 90
Szathmáry, Eörs 72–3, 74–5, 142 Gaia hypothesis and 111–12
Szilard, Leo 151 genes as information 64, 107
group selection 13, 39–40, 41–2
Tarnita, Corina 123–4, 132–3, 134 Huxley’s influence on 112–13
teleology 81, 82–9, 103–4 inclusive fitness 129–30
tempered realism 101–3 length of genes 53
Tennyson, Lord 112 Natural Selection: Domains, Levels and
Tinbergen, Niko 43, 44, 155, 187 Challenges 24, 64, 99
Tooby, John 167, 175, 176–7 neo-Paleyan biology 24
Toxoplasma gondii 158 parsimony 13, 42
Trafalgar, Battle of 11 replicators and vehicles 57, 61–2,
transitions, major 72–8, 142–3 100–1
transitions in individuality 72, 73–4 selfish genetic elements 175
transposable elements 165, 166, 170–1, Wilson, David Sloan 76, 96, 114
172, 173 Wilson, E.O. 37, 43, 80, 111, 117, 123–4,
Trivers, Robert 12, 43, 117, 167, 174, 182 132–3, 134
Wimsatt, William 48, 98
uniparental inheritance 167–8 Wright, Sewall 13, 25–6, 37,
unity of purpose 16, 119, 136, 140–3, 177–8 92–3, 98
Unweaving the Rainbow (Dawkins) 34–5, Wynne-Edwards,Vero Copner 21, 37–8,
93, 111 40, 41, 76
Van Cleve, Jeremy 144–6, 149 X chromosome 89, 164–5

van Valen, Leigh 80
vehicles see replicators and vehicles yeast flocculation 162–3
verbal-conceptual models 186–7
vitalism 55 Zuk, Marlene 116

The Genes Eye View of Evolution

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What is the book about?

What is the book about?

What are some of the criticisms of the selfish gene concept mentioned?

What are some of the criticisms of the selfish gene concept mentioned?

OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi

TH E GEN E’S -­E Y E VI EW

Praise for The Gene’s-Eye View of Evolution:

‘Science needs ingenious points-­of-­view that help us understand

One of my biggest embarrassments in life is that I am such a poor

me from some embarrassing misunderstandings. They did not always

Introduction: A New Way to Read Nature 1

4.3 The gene’s-­eye view and inclusive fitness: equivalence

Introduction: A New Way

T here really is something special about biology. The French bio-

2 T h e Ge n e’s-Ey e V i ew of Evolut ion

I n t roduct ion: A n ew way to r e a d natu r e 3

4 T h e Ge n e’s-Ey e V i ew of Evolut ion

we mean by causality in evolutionary explanations. T he gene’s-­eye

How to think like a selfish gene

The gene’s-­eye view occupies a peculiar position within theoretical

Dawkins’s statement contains the essence of the gene’s-­eye view:

I n t roduct ion: A n ew way to r e a d natu r e 5

not organisms or groups, are the ultimate beneficiaries of nat­ural

In Noble’s version the organism is in control; genes are passive prison-

6 T h e Ge n e’s-Ey e V i ew of Evolut ion

Aims and outline of the book

I n t roduct ion: A n ew way to r e a d natu r e 7

conducted in the philosophical literature, which has meant that many

8 T h e Ge n e’s-Ey e V i ew of Evolut ion

particularly prominent in the United Kingdom and I trace this back

I n t roduct ion: A n ew way to r e a d natu r e 9

10 T h e Ge n e’s-Ey e V i ew of Evolut ion

in particular related to social behaviour. It also helped launch new

12 T h e Ge n e’s-Ey e V i ew of Evolut ion

across it in an internal memo that reported a conversation between

H istor ica l or igi ns 13

1.2 Adaptationism and the legacy

The biological tradition of adaptationism owes much to the field of

14 T h e Ge n e’s-Ey e V i ew of Evolut ion

assumption that the study of the natural world allows inferences to be

H istor ica l or igi ns 15

1.2.1 Why William Paley matters

16 T h e Ge n e’s-Ey e V i ew of Evolut ion

particular, Paley relied extensively on the work of the Dutchman

In crossing a heath, suppose I pitched my foot against a stone and were

Gardner (2009) describes how Paley’s conception of design stands on

H istor ica l or igi ns 17

Just as early Anglican natural theologians were successful partly

18 T h e Ge n e’s-Ey e V i ew of Evolut ion

1.2.2 Neo-­Paleyan biology in Britain

H istor ica l or igi ns 19

When Darwin entered Christ’s College, Cambridge, to prepare for

I am convinced that I could have written out the whole of the

Similarly, short after the publication of the Origin, Darwin wrote in a

20 T h e Ge n e’s-Ey e V i ew of Evolut ion

new field of evolutionary biology in a rather frictionless way

H istor ica l or igi ns 21

London, which to this day lacks a divinity department.) In a letter to

Paley shines through also in the writings of the next generation of

22 T h e Ge n e’s-Ey e V i ew of Evolut ion

TH E GEN E’S -E Y E VI EW

‘Science needs ingenious points-of-view that help us understand

Introduction: A New Way to Read Nature 1

4.3 The gene’s-eye view and inclusive fitness: equivalence

we mean by causality in evolutionary explanations. T he gene’s-eye

The gene’s-eye view occupies a peculiar position within theoretical

Dawkins’s statement contains the essence of the gene’s-eye view:

not organisms or groups, are the ultimate beneficiaries of natural

1.2.2 Neo-Paleyan biology in Britain

Taken together, the gene’s-eye view owes to natural theology in

1.3.2 Fisher (1918) and the birth of the gene’s-eye view

1.3.4 The gene’s-eye view and the Fundamental

The third strand of evolutionary thought that the gene’s-eye view

1.4.1 Wynne-Edwards and the origins

ecology and evolution, underlies organismic and developmental biology,

Nevertheless, Wynne-Edwards, who read zoology at New College,

when the short-term advantage of the individual undermines the

As the author of numerous best-selling books and presenter of