Review TRENDS in Ecology and Evolution Vol.21 No.

1 February 2006

Diversity and flexibility of sex-change

strategies in animals
Philip L. Munday1, Peter M. Buston2 and Robert R Warner3
1
Centre for Coral Reef Biodiversity, School of Marine Biology and Aquaculture, James Cook University, Townsville,
Qld 4811, Australia
2
National Centre for Ecological Analysis and Synthesis, University of California, Santa Barbara, CA 93101-5504, USA
3
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106-9610, USA

Here, we review recent empirical advances that have the hypothesis is often presented as a plot of expected
improved our understanding of why and when sex fertility against body size for males and females (Figure 1).
change occurs. We show that sex-changing animals use Sex change is favoured where fertility increases more
a greater diversity of strategies to increase their quickly with size (or age) for one sex compared to the
reproductive success than was previously recognized: other, assuming that growth and mortality rates are
some individuals change sex early, others change sex approximately the same for both sexes. Sex change is
late, some individuals change sex more than once, and predicted to occur at the size or age where the fecundity
others do not change sex at all. These different gain curves of the sexes intersect [4] (Figure 1).
strategies can be unified by the principle that individuals In an attempt to understand variation in the timing of
change sex when it increases their reproductive value. sex change, Warner [5] suggested that the SAH be framed
The breeding tactics (male, female or non-breeder) in terms of the reproductive value of each sex rather than in
adopted by individuals often appear to be adaptive terms of fertility. Reproductive value (RV) is expected
responses to their own social–ecological context and future reproductive success, taking into account effects of
variation in these conditions results in significant growth and mortality. By using RV, the SAH can take into
differences in the timing of sex change within and account sex-specific differences in expected growth, mor-
between species. tality and chances of obtaining high levels of reproductive
success later in life. The size-advantage prediction then
becomes that sex change should occur at the size where the
Introduction male and female RV curves intersect (even if current
Sex allocation theory explains the way in which organisms fertility declines). Framing predictions in terms of sex-
allocate resources to male and female function [1]. The specific RV helps explain why the timing of sex change does
theory encompasses issues ranging from offspring sex- not always correspond with predictions based solely on sex-
ratio adjustment by gonochores (which have fixed sexes) to specific fertility [6]. It also predicts that individuals from
allocation to male and female function by hermaphrodites the same population might change sex at different sizes
(which can have both sexes during their lifetime). because of the different ways that they can trade off sex-
Hermaphrodites are typically classified as either simul- specific fertility, growth and mortality [7].
taneous, where individuals function as male and female at The first mathematical formulations of the SAH were
the same time, or sequential, where individuals first population genetic models, where the direction and timing
function as one sex and then swap to the other sex at some of sex change were viewed as evolutionary responses to
later stage (sex change; Box 1). For simultaneous demographic parameters of the entire population (i.e. size-
hermaphrodites, sex allocation theory is used to predict specific fecundity, mortality and growth) [4]. These models
the optimal allocation an individual should make to male predict a single optimal size at sex change within a
and female function. For sequential hermaphrodites, sex population. However, the SAH can also be applied at the
allocation theory focuses on explaining why individuals scale of the local mating group. This is applicable
change sex and predicting when they should do so. in situations where sex change is a phenotypically plastic
Sex change occurs in animals as diverse as annelids, response to local conditions [5], which is evidently the case
echinoderms, crustaceans, molluscs and fishes [2]. One in the many species where sex change is socially controlled
part of sex allocation theory, the size-advantage [8,9]. In this situation the advantage of sex change for any
hypothesis (SAH) [3,4], is widely used to understand sex individual is based on its RV as male or female relative to
change [1,4]. The SAH predicts that sex change is the size of the other individuals in the mating group.
favoured when an individual reproduces most efficiently Expectations of sex-specific growth, mortality and fertility
as one sex when young or small, and most efficiently as the can vary from one local social group to another, and
opposite sex when old or large [3,4]. In its simplest form, changes in circumstances can rapidly alter these expec-
Corresponding author: Munday, P.L. ([email protected]).
tations. Consequently, we expect to find adaptive variation
Available online 14 November 2005 in the timing of sex change within populations as a result
www.sciencedirect.com 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.10.020
90 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006

Box 1. What is sex change?

Adult sex change occurs when an individual changes from one [47], just as adult sex change is in many species. It now seems that
functional sex to the other. Although this definition is relatively there could be a continuum in the timing of sexual differentiation in
simple, the sexual patterns of hermaphroditic animals are often some species that transcends ontogenetic boundaries. In this
complex and difficult to categorize [61,62]. For example, small fishes perspective, individuals choose to become male or female at various
from the genus Lythrypnus can have mature gametes of both sexes in crucial stages throughout their lives, with adult sex change simply
the gonad, but individuals appear to function exclusively as one sex or being the last stage in the process.
the other [63]. Anatomically, they resemble simultaneous herma-
phrodites, but functionally they are sequential hermaphrodites. The
distinction between anatomy and function is important because sex
allocation theory considers the way that fertility curves of the sexes (a) (b)
scale with size, age, or available resources [1]. Thus, it is reproductive
output (function) of each sex that really counts when assessing the
adaptive significance of hermaphroditism.
From an ontogenetic perspective, adult sex change is just one part
of the sex determination process. Individuals of many species can also
make choices about being male or female before maturation. Consider
a classic protogynous (female first) hermaphrodite: individuals begin
life as juvenile females, they mature into adult females, some of which
change sex to become adult males. In some species, such as the
bluehead wrasse Thalassoma bifasciatum [12] (Figure I) and Figure I. Complex life histories of sex-changing animals. This is illustrated by the
bluehead wrasse Thalassoma bifasciatum where individuals can mature as either
the humbug damselfish Dascyllus aruanus [64,65], a proportion of
a female or a primary male. Females and primary males look almost identical (a).
the juveniles become males without first breeding as a female (these
Adult females change sex when they have the opportunity to take over the
are usually called primary males). Even more complex patterns exist: territory of a large male. Females that change sex and become a territorial male
juvenile Gobiodon can mature directly into either adult males or adult take on a distinct, bright colouration (b). Primary males can also become brightly
females [66], both of which are capable of subsequent sex change [50]. coloured if they reach a size large enough to defend a territory, even though they
Importantly, recent research has shown that the decision to become have not changed sex. Photographs reproduced with permission from Will White
a primary male might be a plastic response to local social conditions and Ken Clifton.

of variation in the size structure and dynamics of different randomly with regard to size [6,15–17]. The message
mating groups. from the empirical data is that interspecific differences in
Here, we review recent empirical developments that the direction of sex change (protogyny versus protandry)
have improved our understanding of why and when sex are often associated with differences in the mating system.
change occurs. We show that sex-changing species exhibit Empirical evidence also suggests that the mating
a greater diversity of sexual strategies than previously system, or mating group structure, influences the relative
recognized, and that individuals appear to tailor the timing of sex change between species. In a recent study,
timing and direction of sex change to maximise their RV. Collin [18] found significant variation in the relative size
We also show that variation in the timing of sex change at sex change (average size at sex change divided by
among species, populations and individuals can often be maximum size) of 19 species of protandrous gastropods.
traced back to differences in the structure of the local This result contrasts with earlier reports that the relative
mating group. Our conclusions contrast with recent size at sex change is the same (i.e. invariant) in all sex-
analyses that have proposed that sex change occurs at changing species [10,11]. At least part of the reason for
the same relative size across species [10,11] and demon- these conflicting results appears to lie in the method that
strate that understanding the scale at which individuals has been used to test invariance (Box 2), which obscures
gather information on RV is crucial to our understanding
of the selective advantage of sex change. (a) (b)

The mating system and variation in the timing

of sex change
Fertility

The mating system provides the opportunity for the RV of

males and females to increase with size at different rates.
In polygynous mating systems, where large males
monopolize matings with many females, male RV is
strongly dependent on size. This favours female–male
Body size Body size
sex change (protogyny). When the mating system
is known, most species exhibiting protogyny have a TRENDS in Ecology & Evolution

polygynous mating system [12,13]. By contrast, in Figure 1. The size advantage hypothesis. Expected female offspring production (blue
monogamous systems or where mating is random, female line) increases with body size if large females can lay more eggs. Expected male
RV tends to be more strongly dependent on size than offspring production (red line) increases strongly with body size if, for instance, large
males breed with many more females than do small males. Sex change is favoured
does male RV. This favours male–female sex change when the size- (or age-) specific fertility curves of the sexes cross. Female–male sex
(protandry). Although the mating systems of most change [(a) protogyny] is favoured when the fertility of an average male increases
protandrous sex changers are not well described, species more rapidly than the fertility of an average female. Male–female sex change
[(b) protandry] is favoured when fertility of an average female increases more rapidly
for which the mating system is known are either than fertility of an average male. Fitness functions can be applied at the scale of the
monogamous [14] or appear to mate approximately breeding group or at the scale of the breeding population (as appropriate).

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 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006 91

Box 2. An invariant size at sex change?

The life-history invariant approach to the study of life-history life-history trait constrains the other [21]. So, how do we identify
evolution [67] has generated much interest. The approach tests invariance? One suggestion is to compare variation in potentially
hypotheses that dimensionless ratios of life-history traits are invariant invariant traits to variation in other traits [20]; however, what sort of
across populations or taxa. The existence of invariance is interesting traits could be compared, and what range of variance would qualify for
because it suggests that there is a general explanation for the invariance, has yet to be defined.
evolution of the invariant trait. Recently, two studies [10,68] have Another question is when will an invariant pattern be informative?
suggested that the relative size at sex change is invariant across Allsop and West [10,68] suggested that, across species, average size at
taxa. An ensuing debate has questioned the validity of these claims sex change divided by maximum size of the species is invariant. This
and, indeed, the whole approach used to detect life-history invariance implicitly assumes that there is a single optimal size at sex change in
[19–21,69]. each species. Although this assumption is probably valid for some
The claim that relative size at sex change is invariant is based on the populations [70], it is probably not true for populations with distinct
observation that a log-log plot of average size at sex change against mating groups. Populations are often subdivided into breeding
maximum size produces a slope of 1 and a high R2 [10]. However, null groups and optimal size at sex change varies among these groups,
models, in which size at sex change is randomly distributed between depending on the size structure and social conditions experienced
size at maturity and maximum size, produce the same apparent in each group. In such cases, the sex-change rule (or invariant)
invariance in relative size at sex change [19,20,69] (Figure I). This will probably be found by comparing groups rather than whole
seems to be a general problem for claims of invariance in which one populations or species.

(a) (b)
8 8

Average size at sex change (natural log)

7 7

6 6
Number of species

5 5

4 4

3 3

2 2

1 1

0 0
0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95 1.00 0 1 2 3 4 5 6 7 8
Relative size of fish at sex change Maximum body size (natural log)

(c) (d)
5
8
Average size at sex change (natural log)

7
4
6
Number of species

3 5

4
2
3

2
1
1

0 0
0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95 1.00 0 1 2 3 4 5 6 7 8
Null relative size of fish at sex change Maximum body size (natural log)

TRENDS in Ecology & Evolution

Figure I. Variation in the relative size at sex change among species. (a) Relative size at sex change for 52 species of fishes. Relative size at sex change is the average size at
sex change recorded for a species divided by maximum body size of the species. (b) These data appear invariant (slope of 1 and high R2) when the average size at sex
change is plotted against maximum size on a log-log scale. However, null data, where the relative size at sex change is randomly distributed (c) also produce an
apparently invariant relationship when plotted on a log-log scale (d). Data taken from [68] (a).

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92 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006

much of the interesting variation in the timing of sex Within-population variation in the timing of sex change
change [19–21]. Importantly, a large amount of the Not all individuals in a population of sex-changing
variation in size at sex change among species observed animals follow the same life history. In some species, a
by Collin [18] was associated with variation in mating proportion of the population matures directly into the
group structure. This indicates that variation in social second sex (Box 1). Other individuals never change sex
structure can indeed drive differences in the timing of sex because favourable conditions do not arise. More intri-
change between species. guing are individuals that change sex when there is no
One of the most dramatic effects of the mating system immediate advantage in doing so, dominant individuals
on the timing of sex change is seen in species with that do not change sex when the opportunity arises, and
alternative male tactics, such as the bluehead wrasse individuals that change sex more than once. RV provides
Thalassoma bifasciatum. Where local conditions favour the key to understanding this variation in the timing and
resource defence polygyny, most males are derived by direction of sex change.
adult sex change [12,22]. By contrast, when high
densities make resource defence polygyny uneconomic, No sex change
individuals usually choose to become male before In haremic species, the largest female in a group usually
maturation (so-called primary males; Box 1) [12,22] and changes sex following the disappearance of the dominant
never change sex as adults. Differences in the relative male [5,12,13,33] because she can increase her RV by
frequency of sex change can occur on neighbouring reefs, spawning with all the remaining females. Some females
indicating that individuals are choosing a life-history even change harems to advance their position in the size
tactic that involves adult sex change, or not, depending hierarchy, and in doing so increase their RV because they
on the mating conditions that they experience in that end up monopolizing a harem sooner [34]. Similarly, in
habitat patch. species that exhibit resource defence polygyny, a large
female will usually change sex following the disappear-
Between-population variation in the timing ance of a territorial male [35] because it greatly increases
of sex change her RV. Territorial males can spawn with O50 females per
The SAH predicts that sex change will occur earlier in day [22], so the advantage to changing sex when a
populations with slower growth rates and/or higher dominant position becomes available can be significant.
mortality rates [5]. This pattern has been documented in It is not always the largest female that changes sex
a range of protogynous [23–25] and protandrous species following the disappearance of a dominant male. This
[26,27], and recent analyses are uncovering the mechan- appears non-adaptive, because the largest female could
isms responsible for this variation. The mean age at sex spawn with all the remaining females if she did change
change and demographic rates co-vary in genetically sex. However, a recent modification of the SAH [36] shows
connected populations of fishes [25,28] and shrimp [26], that the largest female in a group would not increase her
indicating that the timing of sex change in these RV by changing sex if the combined fecundity of the other
populations is a flexible response by individuals to local females in the group is less than her current fecundity,
conditions. This conclusion is supported by the relatively and/or if sperm competition was intense. Under these
rapid changes (within a few years and less than one circumstances, the larger individual would do better to
generation) in the age or size at sex change in some fish remain female and one of the smaller females might gain
populations following a change in the mortality rate [29]. the most by changing sex. These predictions were borne
It is unknown if individuals in any of these populations out in a manipulative experiment with the bucktooth
are responding directly to demographic rates (growth or parrotfish Sparisoma radians, where the largest female
mortality), or to the size distribution of other individuals usually declined to change sex following the removal of the
in the population (a pattern generated by growth and dominant male, and it was one of the smaller females that
mortality rates). However, the results demonstrate that became male [37]. It remains to be seen whether a similar
individual plasticity in the timing of sex change can response occurs in other species where size–fecundity
generate significant structure in the mean size or age of skew and sperm competition might favour large individ-
sex change at large spatial scales. uals that do not change sex. Nevertheless, this example
Although individual plasticity explains variation in the suggests that individuals of some species make precise
size of sex change among populations of some species, assessments of RV and refrain from changing sex when it
evidence suggests that other species have a relatively is not beneficial.
fixed size at sex change. In at least one protandrous
shrimp [30] and one protandrous limpet [31], there was no Early and late sex change
variation in size at sex change despite considerable short- Females sometimes change sex at a size where they
term variation in age structure and mortality rates within appear to have little chance of breeding as a male (early
and between populations. The apparent absence of sex- sex change) and thus experience no immediate gain in
ratio compensation following selective removal of males by reproductive success [38,39]. Early sex change might be a
fishing in some large protogynous fishes [32] suggests that viable alternative strategy if non-reproductives have
they also have a relatively fixed size at sex change. Why decreased mortality rates or increased growth rates [7],
the timing of sex change should respond strongly to local so that a small decrease in current reproductive success
environmental conditions in some species, but not others, results in a much larger gain in RV. Early sex change in
deserves further attention. the spotlight parrotfish Sparisoma viride appears to be
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 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006 93

favoured because non-reproductive males grow faster

than do territorial males [40] and do not appear to suffer (a) (b)
markedly higher mortality rates [41]. Simple multipli-
cations of size-based fecundity and number of spawns per
year indicate that the lifetime fecundity of early sex
changers is similar to that of individuals that change sex
later in life [41]; thus, early sex change can be a viable
alternative breeding tactic in this species.
An alternative reason for early sex change is that these
individuals have the best chance of taking over a harem, Figure 2. Examples of fish that change sex. Monogamous coral gobies and
or breeding territory, following the loss of a territorial anemonefishes are ecologically similar but exhibit different sexual patterns. (a)
Bidirectional sex change is beneficial in the coral goby Gobiodon histrio because
male [42]. Here, there is not necessarily a growth or movement between corals might be required to form a breeding pair following the
survival advantage to early sex change; individuals are loss of a partner. The ability to change sex in each direction enables an individual to
simply positioning themselves to take over from a breed with any other single adult encountered, and thus reduce the risk of
searching for a new partner [49,50]. (b) Bidirectional sex change does not occur in
territorial male [43]. The probability of encountering a the anemonefish Amphiprion percula, because the replacement mate is always
vacant territory increases in circumstances where many from non-breeders within the anemone [14]. Movement to find a new partner is an
such territories can be sampled, and it is in these option for coral gobies because the habitat patches that they occupy tend to occur
in much higher density than those used by anemonefishes. (b) reproduced with
circumstances that large females of some species of permission from Shane Paterson.
angelfish and parrotfish abandon reproduction, change
sex and become roving bachelor males. Where opportu- the breeding pair dies (or the host coral dies) the survivor
nities are more restricted, large females remain in a might move to find a new partner. Searching for a new
harem and do not change sex before the dominant male mate is, however, risky [49,50]. When new partnerships
position becomes vacant [44]. form, one individual will change sex if the new partners
In some cases, individuals delay sex change to increase are the same sex. The advantage of bidirectional sex
their RV. The protandric hermaphroditic shrimp Lysmata change is that an individual maximizes its RV by
wurdemanni lives for !18 months and individuals searching as little as possible for a new mate [49,50]
reproduce in only one or two breeding seasons [45]. (Figure 2).
Males that recruit to the population early in the season Repetitive sex change also occurs in polygynous
change sex to female after a few months. By contrast, species. In the small reef fish Trimma okinawae, proto-
males that recruit later in the season do not sex change gynous sex change occurs when a female becomes the
until the start of the next breeding season. Late recruiters largest individual in a social group. Males can change
apparently delay sex change because they have a growth back to female if they change social groups and
or survival advantage as males during the winter non- find themselves subordinate to a larger male [52].
reproductive period [45]. Unpredictable changes in group structure are likely to
occur in species such as T. okinawae, because their small
Repetitive sex change size (they are among the smallest vertebrates) makes
It has been known for a long time that repetitive sex them highly vulnerable to predation. Furthermore, the
change can occur in some invertebrates [1,2], but sex short life span of small gobies (sometimes just a few
change in vertebrates was thought to occur just once, months [53]) means that any delay in finding a breeding
either because there were physiological constraints on sex partner might seriously diminish the RV of an individual.
reversal, or because there was no advantage in reverting Thus, the expense (mortality risk and lost mating
to the original sex. This assumption has been overturned opportunities) incurred by a single male waiting for a
by an increasing list of fish species in which multiple sex dominant position to become available following loss of a
reversals can occur ([13,46–48] and references therein) harem is likely to exceed the cost of changing sex and
and by the recognition of ecological conditions that favour breeding as a female in an existing group.
repetitive sex change [49,50]. In some species, repetitive sex change has not been
The polychaete worm Ophryotrocha puerilis forms observed in the wild, despite the capacity for sex change
breeding pairs. In each pair, the largest individual in each direction being demonstrated in laboratory
functions as a female, enabling individuals to take experiments [54]. Future research should concentrate on
advantage of the female size–fecundity relationship. elucidating where and when repetitive sex change occurs
Males grow more quickly than do females and reciprocal in nature.
sex change occurs when the male becomes larger than the
female. This enables the pair to continue to maximize
their reproductive success over multiple breeding bouts Proximal cues and variation in the timing of sex change
[51]. In this system, the fact that the relative size of We have shown that individuals generally change sex
individuals in a pair changes over time creates a benefit when it increases their RV. What cues do they use to assess
for repetitive sex change. the RV of being male or female, and how does this
Monogamous coral gobies also exhibit repetitive sex influence variation in the timing of sex change?
change, but the benefit of this strategy is not related to the Experiments have confirmed that the timing of sex
relative size of individuals in the pair, and reciprocal sex change is sensitive to the immediate social environment in
change has not been observed. In coral gobies, when one of limpets [9,55], snails [56], shrimp [17] and many species of
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94 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006

fish [8,12,13,33]. The size of an individual relative to Understanding the benefits of sex change to individuals
others in the social group [14,35,55], the sex ratio of the is key to understanding its adaptive significance. This
social group [9,50,57] and local density [58,59] have all will require detailed information about sex-specific
been shown to influence the timing of sex change. Clearly, fecundity, growth, mortality and movement patterns at
each of these factors can provide reliable information on the individual level. Only then can we really assess how
the probable success of an individual as one sex or RV is affected by the different breeding tactics (male,
the other. female or non-breeder) that individuals can use. We
Selection could favour simple decision rules for sex predict that a multiplayer game theoretic approach (e.g.
change, based on a single cue such as relative size, sex [60]) will prove useful for modelling the advantage of sex
ratio, or density, if one cue is a reliable predictor of sex- change in species where this trait is under social control.
specific RV. For example, anemonefish have highly Such models could compare the RV of different breeding
predictable social hierarchies, where changing sex to tactics for a range of different social and ecological
female is advantageous when a male becomes the largest conditions. Models that can be applied at the scale of
individual in a social group. In this circumstance, a individuals and that can incorporate a diversity of factors
simple rule of thumb about when to change sex (e.g. that influence current and future reproductive success are
when largest in a group) will usually lead to an increase the way of the future.
in RV. Selection could, however, favour a more complex
decision algorithm based on multiple cues, if several Acknowledgements
factors have a major influence on sex-specific RV. In Chris Petersen, Stuart West, Howard Choat, Geoff Jones, Mark
the basslet Pseudanthias squamipinnis, the largest McCormick, Yvonne Sadovy, Colleen Webb, Marian Wong, Stefan Walker
individual adopts male sex in small groups, but as and anonymous referees provided helpful comments on the article. We
also thank Will White, Ken Clifton and Shane Paterson for photographs,
group size grows (and sex ratio becomes female biased) and the Australian Research Council, Fulbright Commission, Partner-
additional individuals might benefit from becoming male ship for the Interdisciplinary Study of Coastal Oceans, and National
[57]. In this situation, relative size and sex ratio act as Centre for Ecological Analysis and Synthesis for financial support.
cues to sex change. As the social situations that
individuals encounter become more varied, selection References
might favour more complex algorithms governing the 1 Charnov, E.L. (1982) The Theory of Sex Allocation, Princeton
timing of sex change. University Press
Variation in the cues that individuals use to make 2 Polikansky, D. (1982) Sex change in plants and animals. Annu. Rev.
Ecol. Syst. 13, 471–495
decisions about sex change will influence variation in the
3 Ghiselin, M.T. (1969) The evolution of hermaphroditism among
timing of sex change, within and among populations. animals. Q. Rev. Biol. 44, 189–208
The greatest variation should occur in populations where 4 Warner, R.R. (1975) The adaptive significance of sequential hermaph-
the size structure, sex ratio, or density of local social roditism in animals. Am. Nat. 109, 61–82
groups varies greatly. Even the simplest algorithms about 5 Warner, R.R. (1988) Sex change and the size-advantage model. Trends
Ecol. Evol. 3, 133–136
when to change sex can generate significant variation in 6 Collin, R. (1995) Sex, size, and position: a test of models predicting size
the timing of sex change if there is variation in the at sex change in the protandrous gastropod Crepidula fornicata. Am.
structure of local social groups. Nat. 146, 815–831
7 Iwasa, Y. (1991) Sex change evolution and cost of reproduction. Behav.
Conclusions Ecol. 2, 56–68
8 Shapiro, D.Y. (1987) Differentiation and evolution of sex change in
Empirical studies are revealing surprising variation in the fishes. Bioscience 37, 490–497
timing of sex change within and between species. In most 9 Collin, R. et al. (2005) Effects of conspecific associations on size at sex
cases, these strategies appear to be adaptive when viewed change in three species of calyptraeid gastropod. Mar. Ecol. Prog. Ser.
in the context of the local social and ecological environ- 293, 89–97
10 Allsop, D.J. and West, S.A. (2003) Changing sex at the same relative
ment of an individual. This suggests that individuals are
body size. Nature 425, 783–784
often able to assess the reproductive value associated with 11 Gardner, A. et al. (2005) A dimensionless invariant for relative size at
functioning as one sex or the other, and to adopt the sex change in animals: explanation and implications. Am. Nat. 165,
appropriate breeding tactic. 551–566
Elucidating the proximal mechanisms that control sex 12 Warner, R.R. (1984) Mating behavior and hermaphroditism in coral
reef fishes. Am. Sci. 72, 128–136
change is important because these mechanisms indicate
13 Kuwamura, T. and Nakashima, Y. (1998) New aspects of sex change
the scale at which individuals are assessing RV. In many among reef fishes: recent studies in Japan. Env. Biol. Fish. 21,
species, the timing of sex change varies at the scale of local 125–135
social groups, and this is the scale at which we should 14 Buston, P. (2003) Size and growth modification in clownfish. Nature
examine the selective advantage of sex change. Some 424, 145–146
15 Bauer, R.T. and Abdalla, J.H. (2001) Male mating tactics in the shrimp
other species appear to have a relatively fixed size at sex Palaemonetes pugio (Decapoda, Caridea): precopulatory mate guard-
change, and in these species the advantage of sex change ing vs. pure searching. Ethology 107, 185–199
could be examined at the population level. Other species 16 Shinomiya, A. et al. (2003) Mating system and protandrous sex change
are likely to exhibit interactions between genetic and in the lizard flathead, Inegocia japonica (Platycephalidae). Ichthyol.
environmental sex determination, and will be particularly Res. 50, 383–356
17 Baeza, J.A. and Bauer, R.T. (2004) Experimental test of socially
beneficial to study because they could provide a deeper mediated sex change in a protandric simultaneous hermaphrodite, the
understanding of the multiple scales over which factors marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behav.
influencing RV can operate. Ecol. Sociobiol. 55, 544–550
www.sciencedirect.com
 Review TRENDS in Ecology and Evolution Vol.21 No.1 February 2006 95

18 Collin, R. Sex ratio, life history invariants, and patterns of sex change 45 Baldwin, A.P. and Bauer, R.T. (2003) Growth, survivorship, life-span,
in a family of protandrous gastropods. Evolution (in press) and sex change in the hermaphroditic shrimp Lysmata wurdemanni
19 Buston, P.M. et al. (2004) Sex change and relative body size in animals. (Decapoda: Caridea: Hippolytidae). Mar. Biol. 143, 157–166
Nature 428, doi:10.1038/nature02512 46 Sakai, Y. et al. (2003) Sexually dichromatic protogynous angelfish
20 Nee, S. et al. (2005) The illusion of invariant quantities in life Centropyge ferrugata (Pomacanthidae) males can change back to
histories. Science 309, 1236–1239 females. Zool. Sci. 20, 627–633
21 de Jong, G. (2005) Is invariance across animal species just an illusion? 47 Liu, M. and Sadovy, Y. (2004) The influence of social factors on adult
Science 309, 1193–1195 sex change and juvenile sexual differentiation in a diandric,
22 Warner, R.R. and Hoffman, S.G. (1980) Population density and the protogynous epinepheline, Cephalopholis boenak (Pisces, Serranidae).
economics of territorial defense in a coral reef fish. Ecology 61, J. Zool. Soc. Lond. 264, 239–248
772–780 48 Wittenrich, M.L. and Munday, P.L. (2005) Bi-directional sex change in
23 Cowen, R.K. (1990) Sex change and life history patterns of the labrid, coral reef fishes from the family Pseudochromidae: an experimental
Semicossyphus pulcher, across an environmental gradient. Copeia evaluation. Zool. Sci. 22, 797–803
1990, 787–795 49 Nakashima, Y. et al. (1995) Why be a both-ways sex changer? Ethology
24 Buxton, C.D. (1993) Life-history changes in exploited reef fishes on the
101, 301–307
east coast of South-Africa. Env. Biol. Fish. 36, 47–63
50 Munday, P.L. (2002) Bi-directional sex change: testing the growth-rate
25 Gust, N. (2004) Variation in the population biology of protogynous
advantage model. Behav. Ecol. Sociobiol. 52, 247–254
coral reef fishes over tens of kilometres. Can. J. Fish. Aquat. Sci. 61,
51 Berglund, A. (1986) Sex change by a polychaete worm: effects of social
205–218
and reproductive costs. Ecology 67, 837–845
26 Charnov, E.L. and Hannah, R.W. (2002) Shrimp adjust their sex ratio
52 Sunobe, T. and Nakazono, A. (1993) Sex change in both directions by
to fluctuating age distributions. Evol. Ecol. Res. 4, 239–246
alteration of social dominance in Trimma okinawae (Pisces: Gobiidae).
27 Taylor, R.G. et al. (2000) Age, growth, maturation, and protandric sex
Ethology 94, 339–345
reversal in common snook, Centropomus undecimalis, from the east
and west coasts of South Florida. Fish. Bull. 98, 612–625 53 Depczynski, M. and Bellwood, D.R. (2005) Shortest recorded
28 Gust, N. et al. (2002) Demographic plasticity in tropical reef fishes. vertebrate lifespan found in a coral reef fish. Curr. Biol. 15, 288–289
Mar. Biol. 140, 1039–1051 54 Kuwamura, T. et al. (2002) Reversed sex-change in the protogynous
29 Hawkins, J.P. and Roberts, C.M. (2003) Effects of fishing on sex- reef fish, Labroides dimidiatus. Ethology 108, 443–450
changing Caribbean parrotfishes. Biol. Conserv. 115, 213–226 55 Warner, R.R. et al. (1996) Social control of sex change in the shelf
30 Bergström, B.I. (1997) Do pandalid shrimp have environmental sex limpet, Crepidula norrisiarum: size-specific responses to local group
determination? Mar. Biol. 128, 39–407 composition. J. Exp. Mar. Biol. Ecol. 204, 155–167
31 Branch, G.M. and Odendaal, F. (2003) The effects of marine protected 56 Chen, M-H. et al. (2004) Host effect on size structure and timing of sex
areas on the population dynamics of a South African limpet, Cymbula change in the coral-inhabiting snail Coralliophila violacea. Mar. Biol.
oculus, relative to the influence of wave action. Biol. Conserv. 114, 144, 287–293
255–269 57 Shapiro, D.Y. (1984) Sex reversal and sociodemographic processes in
32 Petersen, C.W. and Warner, R.R. (2002) The ecological context of coral reef fishes. In Fish Reproduction: Strategies and Tactics (Potts,
reproductive behavior. In Coral Reef Fishes: Dynamics and Diversity G.W. and Wooton, R.J., eds), pp. 103–118, Academic Press
in a Complex Ecosystem (Sale, P.F., ed.), pp. 103–118, Academic Press 58 Wright, W.G. (1989) Intraspecific density mediates sex-change in the
33 Ross, R.M. (1990) The evolution of sex-change mechanisms in fishes. territorial patellacean limpet Lottia gigantea. Mar. Biol. 100, 353–364
Env. Biol. Fish. 29, 81–93 59 Lutenesky, M.M.F. (1994) Density-dependent protogynous sex change
34 Sakai, Y. et al. (2001) Effect of changing harem on timing of sex change in territorial-haremic fishes: models and evidence. Behav. Ecol. 5,
in female cleaner fish Labroides dimidiatus. Anim. Behav. 62, 375–383
251–257 60 Alonzo, S.H. (2002) State-dependent habitat selection games between
35 Warner, R.R. and Swearer, S.E. (1991) Social control of sex change in predators and prey: the importance of behavioral interactions and
the bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). expected lifetime reproductive success. Evol. Ecol. Res. 4, 759–778
Biol. Bull. 181, 199–204 61 Sadovy, Y. and Shapiro, D.Y. (1987) Criteria for the diagnosis of
36 Muñoz, R.C. and Warner, R.R. (2003) A new version of the size- hermaphroditism in fishes. Copeia 1987, 136–156
advantage hypothesis for sex change: Incorporating sperm compe- 62 Sadovy, Y. and Domier, M.L. (2005) Perplexing problems of sexual
tition and size-fecundity skew. Am. Nat. 161, 749–761 patterns in the genus Paralabrax (Serranidae, Serraninae). J. Zool.
37 Muñoz, R.C. and Warner, R.R. (2004) Testing a new version of the size- 267, 121–133
advantage hypothesis for sex change: sperm competition and size- 63 St Mary, C.M. (1996) Sex allocation in a simultaneous hermaphrodite,
skew effects in the bucktooth parrotfish, Sparisoma radians. Behav.
the zebra goby Lythrypnus zebra: insights gained through a
Ecol. 15, 129–136
comparison with its sympatric congener, Lythrypnus dalli. Env.
38 Moyer, J.T. and Zaiser, M.J. (1984) Early sex change: a possible
Biol. Fish. 45, 177–190
mating strategy of Centropyge angelfishes (Pisces: Pomacanthidae).
64 Cole, K.S. (2002) Gonad morphology, sexual development, and colony
J. Ethol. 2, 63–67
composition in the obligate coral-dwelling damselfish Dascyllus
39 Hoffman, S.G. et al. (1985) The costs of changing sex and the ontogeny
aruanus. Mar. Biol. 140, 151–163
of males under contest competition for mates. Evolution 39, 915–927
65 Asoh, K. (2003) Gonadal development and infrequent sex change in a
40 van Rooij, J.M. et al. (1995) Plastic growth of the herbivorous reef fish
population of the humbug damselfish, Dascyllus aruanus, in
Sparisoma viride: field evidence for a trade-off between growth and
reproduction. Mar. Ecol. Prog. Ser. 122, 93–105 continuous coral-cover habitat. Mar. Biol. 142, 1207–1218
41 van Rooij, J.M. and Videler, J.J. (1997) Mortality estimates from 66 Hobbs, J-P. et al. (2004) Social induction of maturation and sex
repeated visual censuses of a parrotfish (Sparisom viride) population: determination in a coral reef fish. Proc. R. Soc. Lond. B Biol. Sci. 271,
demographic implications. Mar. Biol. 128, 385–396 2109–2114
42 Aldenhoven, J.M. (1986) Different reproductive strategies in a sex- 67 Charnov, E. (1993) Life History Invariants, Oxford University Press
changing coral reef fish Centropyge bicolor (Pomacanthidae). Aust. 68 Allsop, D.J. and West, S.A. (2003) Constant relative size at sex change
J. Mar. Freshwater Res. 37, 353–360 in sequentially hermaphroditic fish. J. Evol. Biol. 16, 921–929
43 Rogers, L. (2003) Odds-playing and the timing of sex change in 69 Cipriani, R. and Collin, R. (2005) Life-history invariants with bounded
uncertain environments: you bet your wrasse. Behav. Ecol. 14, variable cannot be distinguished from data generated by random
447–450 processes using standard analyses. J. Evol. Biol. doi: 10.1111/j.1420-
44 Warner, R.R. (1991) The use of phenotypic plasticity in coral reefs as 9101.2005.00949x
tests of theory in evolutionary ecology. In The Ecology of Fishes on 70 Charnov, E.L. and Skúladóttir, U. (2000) Dimensionless invariants for
Coral Reefs (Sale, P.F., ed.), pp. 387–398, Academic Press the optimal size (age) of sex change. Evol. Ecol. Res. 2, 1067–1071

www.sciencedirect.com