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and differed in traits other than primary appreciate, however, is that sexual
Primer sexual characters, the differences selection is often stronger than natural
were probably due to natural selection. selection, as it frequently drives trait
Furthermore, whenever a trait is values beyond their naturally selected
Sexual selection developed for the general purposes optima. Furthermore, this occurs even
of life this is also due to natural though sexual selection largely acts
David J. Hosken selection. If, however, a trait provides on only half the population (usually
and Clarissa M. House an advantage over a rival in securing males), a situation that has been
a mate, then it is subject to sexual referred to as the quantitative paradox
Sexual selection is a concept that has selection. Darwin also suggested of sexual selection.
probably been misunderstood and that many characters are likely to be The solution to this apparent
misrepresented more than any other exposed to both forms of selection paradox is that the variance in male
idea in evolutionary biology, confusion and that it will often be difficult to reproductive success is typically
that continues to the present day. We distinguish between the two. But very large, meaning that sexual
are not entirely sure why this is, but although difficult, the distinction is still selection can be strong. It is important
sexual politics seems to have played useful conceptually and operationally, to remember that the variance in
its role, as does a failure to understand and when talking about the sum of reproductive success is a measure of
what sexual selection is and why it was these two mechanisms of evolution, the potential for sexual selection and
initially invoked. While in some ways selection (or net selection) should need not imply that any selection is
less intuitive than natural selection, be used as an umbrella term to occurring the variance in sexual
sexual selection is conceptually incorporate both natural and sexual fitness may be random with respect
identical to it, and evolution via selection and distinguish them from to trait values, which of course means
either mechanism will occur given neutral processes that cause organic no selection. To establish a trait is
sufficient genetic variation. Recent evolution (such as genetic drift). subject to sexual selection, a clear link
claims that sexual selection theory Sexual selection is not a between it and mating success needs
is fundamentally flawed are simply subcategory of natural selection, as to be made (see below). Nonetheless,
wrong and ignore an enormous body Darwin made very clear: it arises from potential and realized selection on
of evidence that provides a bedrock of differences in mating success, whereas male traits is often very strong, with
support for this major mechanism natural selection is due to variance many male characters subject to
of organic evolution. In fact it is partly in all other fitness components. This sexual selection. This includes male
due to this solid foundation that simple delineation comes closest to body size, display rate or display size,
current research has largely shifted Darwins concepts and distinctions. and is why male mammals are often
from documenting whether or not What Darwin apparently did not clearly larger than females, for example.
sexual selection occurs, to addressing
more complex evolutionary questions.

What is sexual selection?


Sexual selection is Darwins second
great insight, and he defined it as
depending on the advantage which
certain individuals have over other
individuals of the same sex and species
solely in respect of reproduction. So
sexual selection can be thought of as
intra-specific reproductive competition.
While some have suggested
distinguishing between sexual and
natural selection is worthless, Darwin
made the distinction clearly, cogently
and for good reason he was trying
to explain the existence of characters
that were apparently not favoured by
natural selection (Figure 1). He says,
for example, that sexual selection
depends not on the struggle for
existence, but on the struggle between
males for possession of females.
Statements like this have been
(mis)interpreted by some as implying
that Darwin was not aware of female Figure 1. Examples of conspicuous sexually selected characters.
These can be display traits used to attract females and/or weapons used in malemale com-
reproductive competition, but this is bat. Shown here (clockwise from top left) are: the plumage of a male sunbird; the exaggerated
clearly not the case. sword of a male sword-tailed fish; the horns of a male chameleon; and the enlarged eye-stalks
Darwin suggested that when males of a male stalk-eyed fly. Images courtesy of Mhairi McFarlane, Nick Royle, Jan Stipala and Sam
and females had different habits, Cotton, respectively.
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Darwin also erroneously suggested not superior, to those of the most and trait would spread through
that promiscuous intercourse will refined and civilized human beings. the population because of this. As
prevent or check the action of sexual Darwin anticipated these arguments Fisher stated Whenever appreciable
selection. We now know that females against female preference, saying that differences exist in a species, which
of most species mate with multiple preference did not depend on a sense are in fact correlated with selective
males and when this occurs there of beauty, but only on females being advantage, there will be a tendency
can be a shift in the focus of sexual able to discriminate amongst males, to select also those individuals of
selection to the post-copulatory so rejection of female preference on the opposite sex which most clearly
arena, resulting in the evolution of this basis represents a fundamental discriminate the difference to be
exaggerated reproductive traits in misunderstanding of choice and observed and this can lead to the
males, such as testis mass. Post- preference in sexual selection. For evolution of male trait and female
copulatory sexual selection is also example, females do not have to be preference.
a major driver of the evolution of actively choosing: if they only mate Fishers fundamental insights were
the male intromittent organ, and on a certain tree, then there will be essentially ignored. In fact it was not
probably sperm form too, but how it selection against any male who is not until some 50 years later that Lande
affects net sexual selection on males also on the tree. This does not require showed that Fishers logic was correct,
is more debatable. Variance in male any higher female cognition, merely and that accelerating evolution of
mating success still appears to be the that because of something females do, preference and trait could occur when
strongest determinant of the strength some male phenotypes do well and the strength of natural selection on
of sexual selection because if a male others do poorly. the male trait was relatively weak
does not mate, he will not take part in Sexual selection was also dealt a and the genetic correlation between
post-copulatory sexual selection. savage blow by Julian Huxley, who female preference and male trait
either did not read Darwin, or did was relatively strong (Figure 2). This
The mechanisms of sexual selection not understand what he had read. work by Lande, together with the
Darwin provided two mechanisms He said for example Darwin further insights of Trivers and others, was
of sexual selection: mate choice failed to draw a general distinction largely responsible for the enormous
and competition for mates. While between interspecific and intraspecific explosion in sexual selection research
acknowledging that males can be selection, although in sexual selection, that has occurred after the early 1970s.
choosy and females competitive, it is as defined by him, he gave the first Sexual selection via female choice
typically females that are more choosy example of intraspecific selection and malemale competition has now
and males that are more competitive, promoting individual success without been documented in many species,
so as a first approximation, mate advantage to the type, and further, and sex-role reversal, where females
choice is female mate choice and display may often be of advantage compete and males are choosy, is also
competition is malemale competition to the species .. and any resultant well documented.
for mates. The logic of this was selection will therefore come under
fleshed-out by Trivers, although the head of Natural Selection. It is Choice for what?
Fisher in letters to A.J. Batemen had abundantly clear from these quotes While it is clear why males are
noted that sexual selection should that Huxley fundamentally failed competing they need females (or
be stronger on males because their to understand Darwins message, more strictly their eggs) to secure
fitness is limited by access to females. but many, including Lack, accepted fitness what is in it for females? The
In any case, Darwins his criticisms, and sexual selection benefits of female choice have been
contemporaries, and those that entered a period of torpor. So much discussed widely and subject to much
followed, readily accepted malemale so that it did not figure in the Modern research. They are broadly divided
mate competition as a mechanism of Synthesis. into direct benefits, increased female
sexual selection, probably because Fisher was the next major figure to fecundity or lifespan, for example, and
malemale competition was so turn his attention to sexual selection, indirect benefits, some increase in the
obvious, but female choice was with a short section in his classic quality of offspring. This quality can
controversial, and confusion about The Genetical Theory of Natural be sexual quality, more attractive sons
female preference/choice continues to Selection. His work explained the (Fishers effect), or general viability
this day. The initial controversy might establishment, spread and persistence (good genes).
be partly because Darwin did not really of female preference, and so filled a Theory has largely focused on
explain why females might have one gap in Darwins original thesis. Fisher indirect benefits perhaps because if
preference over another, or why they imagined a male trait that was initially benefits are direct, there is not a lot
would continue to prefer males with favoured by natural selection. Any left to say females increase their
exaggerated sexual traits. Instead, female that paid attention to that fecundity by mating with specific
Darwin took female preference as a character would have higher fitness males, q.e.d. and Landes model
given, and although he did hint that as her offspring would inherit the trait, assumed no direct selection on
preference could evolve, he at times but also the tendency to pay attention preference. This may, however,
attributed female choice to higher to the trait. Thus, the trait would have inadvertently placed too much
mental faculties. come to have a naturally selected emphasis on the importance of indirect
All this led to the rejection of female advantage and an extra advantage benefits, and empirically there is
mate choice, often through arguments via female preference, which would evidence that direct benefits of choice
of incredulity: it is absurd to credit be proportional to the strength of can be very important. With that in
birds with aesthetic tastes equal, if preference, and both preference mind, some of the most vigorous
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Average strength Measuring sexual selection


of female This is another area that has been
preference Line of neutral
equilibria
subject to considerable debate. In fact,
Grafen asked why we should even
bother to measure sexual selection
at all? The crux of his question was
that Darwins fundamental insight
required no measurement of selection,
plus seeing no sexual selection on a
Lines of motion
character now does not mean it was
not under sexual selection in the past.
There are a number of reasonable
answers to this query, the most
pertinent being that by assessing
selection now, we can infer recent-past
and near-future evolution (if we also
know something about the genetics
involved, because selection does not
always result in evolution).
Measuring current sexual selection
Average size of
male trait is in principle easy, and a framework
for doing this was established over
25 years ago by Lande, Arnold and
Wade. This approach builds on the
simple principle that the selection
operating on a phenotypic trait
can be measured by the statistical
Current Biology
relationship between the trait and
fitness. Lande and Arnold referred
Figure 2. A diagram illustrating Landes model of the Fisher process. to this relationship as a selection
Male trait size (the red tail of the cartoon bird) is plotted on the x-axis and female preference for the gradient, and further showed that the
male tail is on the y-axis. The dotted line (labelled Q) represents the naturally selected optimal tail mathematical form of the selection
size, and female preference tends to move the tail beyond this size. The solid black line (the line gradient tells us how the trait
of neutral equilibria) represents a balance between natural and sexual selection, and when these
two are equal, there is no net selection on tail size. The slope of this line depends on the strength
distribution will change with selection
of natural and sexual selection on tail size. If, for example, female preference is strong and stere- (assuming there is sufficient genetic
otyped and natural selection against exaggerated tail size is weak, the slope will be relatively variation for the trait in the direction of
shallow. The red dotted lines (lines of motion) represent the evolutionary trajectories of a popula- selection), thus providing a useful way
tion, with the precise trajectory followed being determined by the populations starting point. The of characterizing the type of selection
slope of the lines of motion is determined by the genetic correlation between male trait and female targeting a trait.
preference. Shown here is the case when the genetic covariance is relatively strong the lines of
motion have a relatively steep slope and the line of equilibrium has a relatively shallow slope.
In the simplest case, the
This corresponds to Fishers runaway, where populations evolve away from the line of equilibria. relationship between the size of a
Note that above the line of equilibria, larger tails evolve and below it, smaller tails. Redrawn from sexual trait and mating success is
Arnold (1983) in Bateson, P. (ed) Mate Choice (Cambridge University Press, Cambridge). linear, and hence the sign of the
selection gradient indicates whether
debate has been over the importance female phenotype, and finally, inter-locus sexual selection favours an increase
of good genes (for viability) and sexual conflict, the divergence of male or decrease in trait size. This will in
Fishers (attractiveness) sons effect as and female reproductive interests, can turn result in an increase or decrease
indirect benefits of choice. generate direct negative selection on in mean trait expression, with the
Part of the problem is that good female preference. magnitude of this change determined
genes benefits include a sons effect So, in spite of claims that all sexual by the slope of the selection gradient
(as explained by Fisher) and with selection must be inevitably linked and the heritable genetic variation
females exercising some preference, to good genes, this need not be the for the trait. However, selection
male traits will be dragged past their case. We also note here that sexy can also be nonlinear in form. If the
naturally selected optima, so there will sons, which is often confused with relationship between trait and mating
be a viability cost to exaggerated sexual Fishers effect, is in fact the idea that success is concave down, sexual
traits. Furthermore, if male fitness is females can compensate for direct selection will be stabilizing in form
enhanced more by marginal investment negative selection on preferences by and individuals expressing traits
in sexual traits than survival, any positive mating with preferred males females close to the population mean will
link between the size of a male sexual produce fewer offspring through have the highest fitness. Conversely,
trait and male viability will also be lost. the attractiveness of their sons. This if the relationship is concave up,
Additionally, intra-locus sexual conflict, idea has little theoretical support, sexual selection will be disruptive in
sexual differences in optimal trait values, while Fishers sons effect can lead form and individuals with traits at the
may mean good genes for a male to bouts of accelerating evolution of extremes of the distribution will have
phenotype are not good genes for a trait and preference. the highest fitness.
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Based on these criteria, measuring organisms with very different sexual not in their best interests? At this
sexual selection is, in principle, traits. point in time we do not have clear
relatively simple: collect a sample of Numerous researchers have answers to these questions. Even
mating and non-mating males from a taken advantage of this to address more fundamentally, it is currently not
population, measure their phenotype fundamental questions such as what clear if sexual selection is adaptive
and quantify the relationship between is the strength of sexual selection or not. While Darwin invoked sexual
phenotype and mating success. in natural populations? A myriad selection to explain characters that
Unfortunately, however, predicting other statistical approaches have were apparently not adaptive, he
evolutionary responses based on more recently been developed to also suggested sexual selection
assessment of sexual selection is help simplify the interpretation of could lead to the improvement of the
problematic for a number of reasons. nonlinear selection, which can become breed or species, but as Fisher and
This includes Grafens complaint complicated when more than a few Lande explained, sexual selection
failure to detect selection now does traits are being examined, as well often drives traits from their naturally
not mean there was not selection in as to formally compare selection selected optima. Furthermore, if
the past (or future) but additionally, gradients amongst different groups sexual selection inherently includes a
because different traits are nearly (such as populations or the sexes). conflict load, it is also not expected
always correlated with each other These approaches have been used to be adaptive. At present we only
(either at the phenotypic or genetic to address more complex questions have limited evidence bearing on this
level) and selection rarely focuses on such as whether current patterns issue, and because it is only relatively
a single trait at a time, responses to of multivariate sexual selection can recently that we have become aware
selection can differ markedly from explain the evolutionary divergence that sexual selection is a general and
simple expectations. of male sexual traits observed across potent driver of population divergence,
This is illustrated perfectly by the populations and what the relative this is an area ripe for additional work.
fact that sexual selection can also be importance of sexual selection, These are just some issues that
correlational in form if the covariance genetics and drift are to this process. should gain more research time,
between two traits influences mating and we should continue to apply
success. This may occur, for example, Where to now? the multiple regression approach
if two colours on a male birds plumage For much of its early history to sexual selection while also
are preferred most by females when researchers had to collate evidence being aware of the limitation of this
they occur together. This highlights for sexual selection, and establish that approach. These include measuring
the simple fact that sexual selection females (or males) were in fact choosy selection and phenotypes accurately
is a multivariate process. This means and that the outcome of reproductive and meaningfully. Nevertheless, big
that measuring the sexual selection competition was determined by unanswered questions remain for
acting on a given trait is slightly more an individuals phenotype. All this young researchers with an eye for
complicated, as a technique is required established the fundamental truth of detail, and reading Darwin is still a
that enables the direct selection acting Darwins hypothesis, but there are good place to start.
on a trait to be separated from the many areas that still require research
indirect selection operating on it (via and new vistas have appeared as older Further reading
correlations), as well as linear and questions have been answered. Andersson, M., and Simmons, L.W. (2006). Sexual
selection and mate choice. Trends Ecol. Evol. 21,
nonlinear selection gradients to be One area that remains underexplored 298302.
measured independently. is female preference. There is a current Arnold, S.J., and Wade, M.J. (1984). On the
measurement of natural and sexual selection:
Lande and Arnold showed how paucity of information on female theory. Evolution 38, 709719.
some of these issues could in preference functions, their shape, Arnqvist, G., and Rowe, L. (2005). Sexual Conflict
principle be solved using multiple whether there is genetic variation for (Princeton University Press, Princeton).
 Bradbury, J.W., and Andersson, M. (eds) (1987)
regression analysis. By building a them, and the costs of expressing Sexual Selection: Testing the Alternatives (John
regression model that includes the different preferences. This gap restricts Wiley & Sons, New York).
Cameron, E., Day, T., and Rowe, L. (2003). Sexual
suite of correlated male sexual traits our understanding of the nature of conflict and indirect benefits. J. Evol. Biol. 16,
as predictor variables and mating sexual selection acting on male sexual 10551060.
success as the response variable, traits and the evolution of female Darwin, C. (1871). The Descent of Man and
Selection in Relation to Sex (John Murray,
the linear selection gradient for one preference itself. Female reproductive London).
trait can be estimated when the competition is also an area that has Ingleby, F., Hunt, J., and Hosken, D.J. (2010). The
role of genotype-by-environment interactions in
effects of all other correlated traits are received relatively little investigation sexual selection. J. Evol. Biol. 23, 20312045.
held constant. Moreover, by adding and the realisation that sexual-signal Klug, H., Heuschelle, J., Jennions, M.D., and
quadratic terms for each trait and honesty can be compromised by Kokko, H. (2010). The mismeasurement of sexual
selection. J. Evol. Biol. 23, 447462.
the covariance between each pair of genotype-by-environment interactions Lande, R. (1981). Models of speciation by sexual
traits to this linear model, nonlinear also provides fertile ground for new selection on polygenic traits. Proc. Natl. Acad.
Sci. USA 78, 37213725.
selection gradients can be estimated empirical and theoretical research. Mead, L.S., and Arnold, S.J. (2004). Quantitative
when the effects of linear selection We also do not have a clear genetic models of sexual selection. Trends Ecol.
are removed. An additional benefit of understanding of the relative Evol. 19, 264271.

this approach is that, when the traits importance of sexual conflict and
Centre for Ecology & Conservation,
are standardized and mating success traditional sexual selection in driving Biosciences, The University of Exeter,
made relative prior to analysis, the trait evolution. Are females making Cornwall Campus, Tremough, Penryn TR10
selection gradients are directly rational mate choices or are they 9EZ, Cornwall, UK.
comparable across studies using being coerced into choices that are E-mail: D.J.Hosken@exeter.ac.uk