Do Microbes Question Standard Thinking in the Philosophy of

Biology?
Critical Notice of John Dupr
Processes of Life Essays in the Philosophy of Biology

This article has been accepted for publication in Analysis published by Oxford
University Press.

Charlotte Werndl

1. Introduction

This is a highly welcome book that offers a fresh perspective on the philosophy of
biology. It is of interest to both philosophers and biologists and to experienced readers
as well as novices. The book is structured into four sections Science, Biology,
Microbes and Humans and consists of a collection of articles written by John
Dupr over the past few years. A very wide range of topics are discussed. Among
other things, Dupr defends a pluralism that emphasises that while there is only
physical stuff, the kind of things composed of this stuff are fundamentally diverse, a
modest form of social constructivism, the inseparability of science and values, the
thesis of promiscuous individualism that there are various ways of dividing living
systems into organisms, and an anti-reductionist position about biology stating that
complex objects possess properties that are autonomous from properties of their
constituent parts. Dupr also argues that the success in understanding the chemical
basis of genetics has undermined simplistic view of inheritance, that the New
Synthesis is flawed and instead evolutionary theory is a theory in flux, that biological
individuals are typically symbiotic wholes involving many organisms of radically
different kinds and genomes, that cooperation is a characteristic of life, that medicine
has to take seriously the microbial symbiotic relationships, that contrary to
evolutionary psychology human beings are in fact pretty well adapted to modern life,
that in no sense of the word gene can biological legitimacy be given to the concept
of human race, that human nature as something fixed and constant throughout the
human species is an illusion, and that a denial of genetic determinism gives way to a
robust sense of human autonomy.

In the remainder of the review, I will focus on the section on microbes. This is
motivated by Duprs claims that this topic is furthest from the central agenda of the
philosophy of biology (2012: 11) and that attention to microbes demands
reconceptualizations, which are not just a background development but a major
transformation in understanding that needs to be reflected in the philosophy of
biology (2012: 186). The section consists of four papers, three of which are co-
authored with Maureen OMalley (Dupr 2011; OMalley and Dupr 2007; Dupr and
OMalley 2007, 2009). Microbes are defined as organisms too small to be seen
without a microscope. Dupr and OMalley provide a manifesto for the importance of
microbes for the philosophy of biology. They do not disappoint: It is true that the
microbial world has long been neglected in the philosophy of biology and that
attention to microbes offers new conceptual insights and demands revision of, or at
least questions, some widely-held views. On the more critical side, the arguments
sometimes suffer from a lack of clarity and some conclusions could have been better
argued for. In what follows, I will discuss three main claims defended in the section
on microbes, and in order to advance the discussion, I will focus on my objections.
Yet this should not distract from the importance and innovativeness of Dupr and
OMalleys work on microbes, which will hopefully stimulate further research in this
area.

2. A new notion of organism and microbial communities as multicellular organisms

Traditional definitions of multicellular organisms demand that the same genome

appears in differentiated but functionally interrelated cells, thus excluding microbial
communities where there are many different genomes. Yet Dupr and OMalley argue
that a more encompassing definition is suggested by microbes. Because microbial
communities exhibit well-defined organisation and interactions as functional units and
are self-organising entities (Dupr 2012: 172 and 176), they are multicellular
organisms. More generally, Dupr and OMalley complain that the classical notion of
an organism is a problematic biological category and that, in particular, it is an
inferior or even inadequate conception of the medical individual. They demand a
revision of this notion to include microbial communities. In their view, organisms are
whichever cooperative systems of cells are most usefully recognized for exploring
biological function (Dupr 2012: 203). This, they claim, implies that the microbes that
occupy our bodies (such as gut microbes) form part of the human organism.

It is an important point that microbial communities show organism-like properties and

that the biological entities of interest in certain scientific investigations are microbial
communities or include microbial communities. For instance, one would surely want
to agree that for many diseases the entity of concern is not the classical notion of the
human organism but the human body including microbes. So here Dupr and
OMalley fulfil their promise and show that microbes lead to important conceptual
insights in the philosophy of biology.

However, I would have liked to see more careful reflection on what is required from a
definition of an organism. For instance, Dupr and OMalley write:
If communities are self-organizing entities that operate as functional units and are more than simply
aggregations of individuals (Andrews 1998; Ben-Jacob et al. 2000; Kolenbrander 2000), they can only
be excluded from multicellular status if the definition of multi-cellularity is closely based on
knowledge of multicellular eukaryotes. (Dupr 2012: 176)
Why is it that self-organisation, being more than simply aggregations of individuals
and the operation as functional units is a sufficient condition for a multicellular
organism? Similarly, why is it, as the authors argue, that communities which exhibit
well-defined organisation and interactions as functional units should be classified as
organisms (Dupr 2012: 172)? Also, OMalley and Dupr claim:
Many of the characteristics that are used to define multicellularity do not exclude unicellular life when
proper attention is paid to bodies of research that illuminate cellular cooperation, developmental
processes, competition, and communication strategies amongst unicellular organisms. (Dupr 2012:
189)
While they convincingly argue that microbial communities possess many
characteristics of multi-cellular organisms, it is not clear to me why this suggests that
microbial communities are multi-cellular organisms. It could well be that only many,
but not all, of the characteristics of multi-cellular organisms are shown by these
communities.
My view on this matter is that the notion of an organism is a vague concept. Whether
communities that show organism-like properties are called organisms or not is a
matter of convention and is not very interesting. What is interesting are the biological
facts and what entities are most fruitfully employed in certain scientific investigations.
Similar views have been expounded by Griffiths (2012) and, in particular, by Haber
(2013). Haber (2013) in his paper about colonies such as ant or bee colonies also
reminds us that debates about the meaning of organisms have already been around
for a long while. So I think that there are two important insights to be gained from
OMalley and Duprs discussion. First, microbial communities show surprisingly
complex properties and can perform a wide range of functions. Second, in certain
scientific investigations it is most fruitful to employ as basic biological entity a
collective including microbes and not the classical notion of an organism.

Moreover, recall Duprs (2012: 241) doctrine of promiscuous individualism that

there are various ways of dividing living systems into organisms driven by particular
human goals. In my view, promiscuous individualism suggests that both the classical
notion of an organism and the new notion are legitimate concepts, which are useful in
different contexts. However, Dupr and OMalleys discussion gives the impression
that the classical notion of an organism is inferior or even inadequate, leaving me
wonder how this fits to promiscuous individualism. Also, the claim [it] is strongly
suggested by the several lines of research outlined above, that the individual microbe
is not the fundamental ontological unit in microbiology (Dupr 2012: 184) is
puzzling because it seems to suggest that there are fundamental ontological units in
microbiology, which is not in the spirit of promiscuous individualism.

I mentioned above that while Dupr and OMalleys work on microbes is highly
important and inspirational, the arguments could be sometimes clearer. An example is
their response to doubts about conferring the status of an organism to microbial
communities because they lack clear spatial boundaries:
A first response to these doubts might be that clear boundaries are not necessarily connected to
ontological fundamentality. [] Second, the biofilms that are the preferred lifestyle of prokaryotes
make possible their study as bounded multicellular entities as well as contradicting common
conceptions of bacteria as free-floating individuals in occasional and highly impermanent contact.
Finally, there is a large body of empirical work which challenges standard views of boundaries because
it reverses expectations about organismal integrity and microbial ubiquity. In regard to the former, the
omnipresence of genetic exchange in microbial communities shows organism boundaries to be much
more permeable than might have been thought. For the latter [] recent studies taking a more
extensive and finely resolved genomic perspective have found that communities of bacteria and
archaea in hot springs and soils, for example, do actually have geographic limits. (Dupr 2012: 176-
77).
It does not seem clear from this response what position is defended. Is it that clear
boundaries are not important for organismality, as the first point and the point about
organismal integrity seem to suggest? Or is it rather that clear boundaries are
important but that, contrary to what one might think, there are reasonably clear
boundaries also for microbial communities, as the second point and the point about
organismal ubiquity seem to suggest?

3. Doubts about the genetically isolated lineage in the microbial world

Dupr and OMalley question that the genetically isolated lineage, which is often seen
as the fundamental unit of evolutionary theory, has a real analogue in the microbial
world. Their arguments lead to the important insight that there are challenges for the
concept of a genetically isolated lineage that are not present for eukaryotes. In this
sense Dupr and OMalley are right that the microbial world offers challenges to
standard thinking in the philosophy of biology. However, in my view, the claim that
the genetically isolated lineage has no real analogue in the microbial world is still up
to debate (and it might well be that Dupre and OMalley do not disagree with this
sentiment).

Let us look at their arguments in more detail:

It might be possible in principle to construct evolutionary models in which microbial clones play a
similar role to the familiar macrobial lineages. But [] there are some serious difficulties with such
models. The most obvious is timescale. Microbial clones have lifespans of hours or days rather than the
thousands of year typical of macrobial lineages. This suggests a need for higher level models if any
sense it to be made of long-term evolutionary change. It further needs to be decided how the beginning
and end of a clone are to be defined for this purpose, especially in the light of a large body of evidence
that shows little true or enduring clonality in most bacterial populations (Maynard Smith et al. 1993,
2000). The prevalence of mobile genetic elements moving between microbial units again points to a
focus on larger units within which these movements take place. (Dupr 2012: 181)
First of all, their objection about lifespans does not seem to show that for microbes
lineages have no real analogue in the world. Rather, it suggests that other concepts
will be more suitable for longer timespans; for shorter timespans the notion of a
lineage can still be useful. Second, while it is indeed an intricate issue how to define
clones, it is not unreasonable that definitions of clones can be found which are useful
for certain biological investigations, even if none of these definitions is without its
flaws or there is no best definition of a clone. Their third point is about lateral gene
transfer the transfer of genetic material from one microbe to another. Lateral gene
transfer indeed poses some problems for the concept of a genetically isolated lineage.
However, it is still up to debate how prevalent such gene transfer is. This is also
emphasised by Sterenly:
In one view, successful gene migration is a rare event. It has happened many times, and many genes in
the genome of bacterial cell lineages have their original ancestors in other lineages. But that is true only
because we are looking at ancient lineages at the summed results of rare events over 3.5 billion years.
Almost all the genes in any given prokaryote clone-line have been replicating together for millions of
generations (Lerat et al. 2005). In another view, lateral gene transfer is pervasive on evolutionary
significant time scales, but it is very rare for core informational genes those responsible for the
machinery of replication, transcription and translation (Brown 2003, Woese 2008). In the most extreme
view, it is such a pervasive feature of prokaryote evolution as to undermine the very idea that
prokaryote evolution is best thought of a branching tree (Bapteste and Boucher 2008; Doolittle and
Bapteste 2007; Martin and Embley 2004). (Sterenly 2011: 90-91)
So only if lateral gene transfer is a pervasive feature of the evolution of microbes does
it seem justified to claim that the lineage has no real analogue in the microbial world.
What Dupre and OMalleys discussion reminds us is that one should be wary of
insisting that lateral gene transfer is sufficiently rare just to prevent serious damage to
lineage-based biology.

4. Cooperation as a criterion for life

After providing an insightful survey about the very different forms of life that exist on
Earth, Dupr and OMalley turn to the question of what constitutes life. The life forms
that exist on Earth are all of the same kind. Life on other planets or based on other
chemicals might be altogether different from what we know and can imagine. Because
of this, one may argue that our theorising about life will be severely limited. While
this is a legitimate worry, we have to work within our constraints. Thus, like Dupr
and OMalley, we should still try our best in understanding life based on the forms of
life we know on Earth.

Among the most widely agreed features of life are the capacity to form lineages by
replication and to exist as metabolically self-sustaining wholes, and Dupr and
OMalley also endorse them as necessary conditions of life (Dupr 2012: 223). In
addition to this, they advance collaboration as highly characteristic of life (2012: 235).
The characterisation they arrive at is that life occurs at the intersection of lineage
formation and (typically collaborative) involvement in metabolism (2012: 227).
According to their analysis, not only cellular entities but also non-cellular entities are
living. For instance, viruses are non-cellular but they should be classified as living
when metabolically active (and as non-living when not metabolically active) (2012:
216). Moreover, Dupr and OMalley complain that the extant literature on life fails
to acknowledge that the entities that form lineages by replication are not the same as
those that form metabolic wholes. For example, human organisms, as standardly
conceived, are lineage-forming entities but are not metabolic wholes because
microbes in our gut form part of the metabolic wholes (Dupr 2012: 207).

Dupr and OMalleys discussion about collaboration is welcome. It teaches us that

collaboration is more widespread than usually acknowledged in the philosophy of
biology. They are also right to stress that for life as we know it the lineage-forming
entities are not the same as the metabolic wholes. Still, I am not sure everyone will be
convinced that collaboration is a highly characteristic of life. Suppose we discover a
distant planet which is inhabited by billions of different organisms that do not engage
in any collaboration, but can reproduce, are metabolically self-sustaining and show all
the other common criteria of life. It may be a judgement call, but some would
probably still want to call such organisms life and thus would not endorse
collaboration as highly characteristic of life. Moreover, when characterising life,
Dupr and OMalley use the notion of a lineage. As discussed above, they doubt that
the notion of a lineage has a real analogue in the microbial world. Given this, it is
somewhat surprising to see that here they use the notion of a lineage without any
concerns.
Furthermore, I would have liked to see more reflection on what is at stake when
assigning to an entity the status of living. What I have in mind are reflections on
questions such as: Life is a vague term in every-day language. So might it not be that
there is no single best characterisation of life but several equally plausible
characterisations? In a similar fashion, when Dupr and OMalley claim:
Although we do not claim to have provided a definition of life, we do believe we have offered a view
of living matter that offers a flexible resource for understanding the many ways in which life can be
organized. (Dupr 2012: 227)
one would like to know more about what exactly they have provided if their aim was
not to provide a definition of life. Related to this, Dupre and OMalley defend
collaboration as highly characteristic for life but not as a necessary condition of life
(Dupr 2012: 225, 227). One might think that either a feature is necessary for life or it
is contingent and thus not that important at all. Their defence of collaboration as
highly characteristic of life does not fit into this scheme. Thus it would have been
helpful to see a discussion about how features can be important for characterising life
even if they are not necessary conditions of life. Also, Dupr and OMalley repeatedly
stress that there is no sharp dividing line between life and non-life (Dupr 2012: 227),
but it is not clear to me that this follows from their characterisation of life.

Dupr and OMalley highlight that their view on cooperation differs from the standard
view in the philosophy of biology. It would be interesting to know more about what
exactly is the difference. Granted, according to the picture painted by Dupr and
OMalley, cooperation is much more widespread than often thought and typically the
units of selection are collections of organisms. Yet what philosophers of biology are
bound to ask is whether their view differs from the widely held conviction that
evolution is a selfish endeavour. Is it just that individual parts are selfish but they
cooperate because this increases their fitness? So we see all this collaboration because
it is (or at least was initially) advantageous for the individual parts. Or do Dupr and
OMalley endorse the more radical view that the individual parts or the cooperative
units are not selfish. Some of their comments such as
Many of these are activities that no individual microbe can accomplish on its own, and the collective
behaviour is often achieved with a cost for individual altruistic micro-organisms (if they are
perceived through the lens of selfishness) (Dupr 2012: 222)
or the unit of selection, the entity in which selfishness may perhaps be expected as
norm (Dupr 2012: 226, my emphasis) do not seem to rule out a more radical
position.

Finally, I have mentioned above that some of the conclusions could have been better
argued for. An example is the following paragraph:
It is clear to us that leaving viruses out of evolutionary, ecological, physiological, or conceptual studies
of living entities, would allow only an incomplete understanding of life at any level (Wilhelm and
Suttle 1999; Weinbauer and Rassoulzadegan 2004; Suttle 2005). This deep and extensive interaction is
too biologically important, from our perspective, to be considered as purely parasitic. Conceived of
collaboratively, cellular life is constantly bathing in a virtual sea of viruses, within and without every
cell, with evolutionarily significant consequences for the past, present, and future of all cellular life-
forms (Bamford 2003: 232). In fact, says virologist Dennis Bamford (2003, 235) it is time to consider
dividing life into two realms: the cellular realm and the viral one. He believes that only by dealing
more thoroughly with a concept of life fully cognizant of the role of viruses will we be able to achieve
an adequate view of life even as it applies to its cellular manifestations. (Dupr 2012: 216).
In this paragraph Dupr and OMalley claim that viruses should be regarded as a form
of life, but arguments as to why this should be the case could be more explicit.

Critical comments aside, this is a ground-breaking and inspiring book, which every
philosopher of biology should have read. Among other important contributions, this
book shows that attention to microbes demands revisions of, or at least questions,
standard thinking in the philosophy of biology. Philosophers of biology can no longer
ignore the world of microbes.

Department of Philosophy, Logic and Scientific Method

London School of Economics and Political Science
Houghton Street, WC2A 2AE London
[email protected]

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