Download Mate choice for indirect genetic benefits: scrutiny of the current

Functional
Ecology 2007
21, 638–644
ESSARY REVIEW
Blackwell Publishing Ltd
Mate choice for indirect genetic benefits: scrutiny of the
current paradigm
J. S. KOTIAHO*‡ and M. PUURTINEN‡
*Department of Biological and Environmental Science, P. O. Box 35, 40014 University of Jyväskylä, Finland,
‡Natural History Museum, P. O. Box 35, 40014 University of Jyväskylä, Finland
Summary
1. Sexual selection through mate choice, and in particular female choice for indirect
fitness benefits for their offspring, is a major paradigm that currently seems to enjoy
almost unequivocal acceptance. A large body of theoretical work has been built to
explain the evolution of mate choice in the absence of direct benefits, and the empiricists
have enthusiastically verified the various assumptions and predictions of the theory.
2. However, the relative importance of mate choice for indirect benefits in comparison
to choice for direct benefits or to other mechanisms of sexual selection such as male–
male competition or sensory exploitation remains a controversial issue, and this seems
to be forgotten in many empirical studies.
3. Here we discuss what mate choice is, and how mating bias resulting from mate
choice can be distinguished from mating biases resulting from other mechanisms such
as male–male competition or sensory exploitation. We will argue that the evidence for
active mate choice for indirect benefits is not as compelling as the current paradigm
suggests, and that the current emphasis on active mate choice for indirect benefits has
resulted in a distorted view of the nature of sexual selection. We emphasize that unlike
the other mechanisms, active mate choice must come with a cost to females.
4. We conclude by suggesting what we feel are three important areas that require
further study before active mate choice for indirect fitness benefits should be concluded.
Key-words: female choice, indirect benefits, sexual selection
Functional Ecology (2007) 21, 638–644
doi: 10.1111/j.1365-2435.2007.01286.x
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Sexual selection is a powerful evolutionary force that
has been the subject of much investigation for the past
150 years – and still is (Darwin 1859, 1871; Fisher
1915, 1958; Bateman 1948; Williams 1966; Trivers
1972; Zahavi 1975, 1977; Parker 1979; Andersson
1982b, 1986a, 1994; Alatalo, Höglund & Lundberg
1991; Kirkpatrick & Ryan 1991; Maynard Smith
1991; Höglund & Alatalo 1995; Jennions & Petrie 1997;
Kotiaho 2001; Kotiaho, Simmons & Tomkins 2001;
Kokko et al. 2002; Tomkins et al. 2004; Andersson &
Simmons 2006; Kokko, Jennions & Brooks 2006;
Qvarnström, Brommer & Gustafsson 2006). It is well
established that sexual selection is indeed one of the
most pervasive forces directing evolution, but throughout
its history there has been one field that is repeatedly
challenged and debated: mate choice (for the most
recent attempt see Dall et al. 2006; Roughgarden, Oishi
& Akca 2006). This debate was started already by
Darwin’s contemporary A. R. Wallace (1889), and with
†Author to whom correspondence should be addressed.
E-mail: [email protected]
the benefit of hindsight, it seems that the development
of the whole field was severely retarded due to criticism
levelled on female choice by J. S. Huxley (1938; see also
details in Cronin 1991). Only after Amos Zahavi
proposed his handicap principle for mate choice in
mid 1970s (Zahavi 1975, 1977), interest towards mate
choice research was renewed again. Also this proposal
received initial opposition (e.g. Davis & O’Donald
1976; Maynard Smith 1976), but it was Zahavi’s
proposal that really started an era of a modelling
frenzy in which all aspects of mate choice were modelled
in many subtly different ways (for a review, see Kokko
et al. 2006).
Around this time also began something that now
looks like a school fight between developers of the
Fisherian theory of runaway sexual selection (sexy son
hypothesis) (O’Donald 1980; Lande 1981; Kirkpatrick
1982; Heisler 1984; Pomiankowski, Iwasa & Nee 1991)
and the developers of the theory of indicator mechanism or, as it is more often called today, the theory of
good genes sexual selection (Andersson 1982b, 1986a,b;
Pomiankowski 1987, 1988; Grafen 1990; Iwasa,
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Journal compilation
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Ecological Society,
Functional Ecology,
21, 638–644
Pomiankowski & Nee 1991; Rowe & Houle 1996;
Kokko 1998; Houle & Kondrashov 2002). During the
1980s and 1990s the evolution of mate choice for
indirect benefits was indeed one of the most popular
targets of mathematical modelling in evolutionary
biology, and the reason may be that it was also one of
the most challenging theories for modellers (Maynard
Smith 1991). Simultaneously with the development of
the mathematical models, a lot of empirical work
emerged trying to verify various assumptions and predictions borne from the theory. It seems that the school
fight between the proponents of the two processes led
to paradigmatic changes in the empirical literature:
there is a sudden increase in heritability of sexual traits
around the time when good genes theories started to
be accepted (Alatalo, Mappes & Elgar 1997). Nevertheless, pitting Fisherian runaway sexual selection
against good genes sexual selection has only recently
started to be settled largely due to the observation that
both sexy son and good genes benefits can result from
a single process of female choice for males with high
breeding value for fitness (Kokko et al. 2002; but see
also Eshel, Volovik & Sansone 2000; Jennions, Møller
& Petrie 2001; Kokko et al. 2003, 2006). The most
recent work suggests that the interpretation of the
outcome – sexy sons or good genes, depends on the
costliness of the choice: if choice is cheap, breeding
value for fitness of the male is predominantly mediated
through the sexiness of the sons but if choice is costly,
breeding value for fitness of the males must include
also other components of fitness (Kokko et al. 2002).
Theories involving the evolution of mate choice for
indirect benefits have been intensively developed over
the past 25 years or so and remain the subject of many
studies. What is often forgotten, however, is that
mating biases and elaboration of male sexual traits will
easily evolve if male traits indicate direct fitness
benefits such as increased fertilization success or territory
quality to females (for a review, see Kirkpatrick &
Ryan 1991). Moreover, elaborate male sexual traits
will also evolve with ease in the absence of direct
benefits if mate choice is not costly (Lande 1981). The
evolution of cost-free mate choice, and mate choice for
direct benefits, was thus non-controversial from the
start and did not offer much theoretical challenge.
Therefore, theoreticians soon started to engage
themselves with the much more problematic issue, that
is, with the evolution of costly mate choice for indirect
fitness benefits through Fisher’s self-reinforcing
process, or through good genes process. Following the
lead of the theoreticians, the empirical scientists have
heavily focused on testing the predictions and assumptions of the models for mate choice in the absence of
direct benefits. It is our view, however, that this almost
exclusive focus on costly mate choice for indirect
benefits may have been misguided. Moreover, it seems
that the theory is so appealing, that we have rushed
into finding supportive evidence for it by blinding our
eyes from alternative, often more simple, explanations.
In this paper, we start by discussing the different
meanings of mate choice and stress the importance of
distinguishing between active mate choice, which we
maintain must come with costs, and other mating
preferences such as passive attraction, which are cost
free. We then argue that there is very little empirical
evidence for costly mate choice and that mate choice
for indirect benefits may not be as frequent as the
common paradigm suggests. We further suggest that
the strong focus on indirect benefits of choice and the
relative neglect of direct benefits of choice and other
mechanisms of sexual selection have resulted in a
distorted view of the nature of sexual selection.
What is active mate choice and is it really so
common?
Choice in general is very hard to define as every action
can be interpreted as being a choice. In studies of the
evolution of mate choice, the concept of choice is
naturally of paramount importance. Therefore, its
definition should not be considered as trivial or something that is only semantic in nature. In the past this
was well recognized and there was vivid discussion
about the nature of mate choice (Janetos 1980; Halliday
1983; Parker 1983; Maynard Smith 1985, 1987; Arak
1988; see also Gibson & Langen 1996), but more
recently active mate choice is often taken more or less
as granted. In a recent review of the mathematical
models of sexual selection through mate choice,
Kokko et al. (2006, p. 49) define mate choice as being
the outcome of the inherent propensity of an individual
to mate more readily with certain phenotypes of the
opposite sex (i.e. mating preference or bias) and the
extent to which an individual engages in mate sampling
before deciding to mate (i.e. choosiness). Kokko et al.
(2006) states that in their treatment, choice will be a
concept pooling preference, which might be cost free,
with choosiness, which is less likely to be so. This
definition of mate choice pooling preference and
choosiness will lead to problems in separating mating
bias due to active mate choice from passive attraction
which arises as a by-product of some other process
such as exploitation of a pre-existing sensory bias (see
for example, Kirkpatrick & Ryan 1991). We argue that
to understand sexual selection it is important to distinguish active mate choice from other processes generating
mating biases.
The problem is how to separate active mate choice
from passive attraction or indeed from male–male
competition. This is not a trivial task since all three,
active mate choice, passive attraction and male–male
competition can lead to identical direct or indirect
fitness benefits. In other words, benefits can tell us
nothing about the underlying mechanisms generating
the mating bias. For example, if there is heritable variation in a male trait that females are passively attracted
to due to some pre-existing sensory bias, females
mated with such male will have sons that are more
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Journal compilation
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Ecological Society,
Functional Ecology,
21, 638–644
attractive and leave more descendants. Females will get
this indirect benefit even if they are only passively
attracted to a trait and do not engage in the costly
process of choosing between different males. Thus, we
feel that the only evidence that can support the existence of active mate choice is an empirical observation
of a cost of choice.
At first glance it may seem that, of course, there is
ample evidence for active mate choice. However, most
of the empirical evidence that has been taken as
support for the existence of mate choice may in fact
be equally consistent with passive attraction. Let us
approach this issue with a simple example of a common
choice experiment in which signals from two or more
individuals are presented for a focal individual, that is
then scored for occurrence of choice. The most common
analysis approach to such data is to compare whether
the mean response of the focal individual differs
between the signals. This is the case, for example, in the
most celebrated text book example of mate choice
(Andersson 1982a) but also in countless other studies
of mate choice (e.g. Branham & Greenfield 1996;
Wagner 1996; Parri et al. 1997, 2002; see also table 6A,
pp. 132 –142 in Andersson 1994). There are also some
exceptions as for most generalizations (e.g. Kotiaho
et al. 1996; Castellano, Rosso & Giacoma 2004). Apart
from the problems of taking association with, or
orientation towards a signal as a proxy for choice of a
mating partner, the most serious potential problem
with such an analysis should be clear: it does not take
into account variation in the detectability of the signals.
The importance of taking into account the detectability of the signal in forming the null hypothesis is
easier to portray with a simple imaginary example of
an auditory signal. Let us assume that there is a trait,
say one second long chirp that females use solely in
order to find a mating partner. Apart from using the
trait to locate males, females pay no attention to the
signal but are equally likely to respond after any chirp.
Let us further assume that there is variation in male
chirping rates. For the sake of this example let us
consider only a population with two male types: a male
type with a chirping rate of one chirp per minute and
another male type with a chirping rate of three chirps
per minute. Given these premises, and the common
analysis portrayed above, it will seem that there is
female choice because the male type with higher chirping
rate will have three times higher mating success than
the other type of male. This is because if such data is
tested against the null hypothesis that each male has
the same probability of gaining a mating (i.e. random
mating) we will inescapably conclude that there is mate
choice for more chirping males. However, in this
particular example the null hypothesis should have
been different; it should have been that each of the
males has the same probability of gaining mating per
signal they produce. The point is that by comparing the
mating frequency of two males and not accounting for
the detectability of the signal, seemingly non-random
mating pattern emerges when mating may in fact be
random when the detectability of the signal is taken
into account. It is relatively easy to see that the null
hypothesis against which the data should have been
tested in this example should have been 1 : 3. This
relative ease of deriving the correct null-hypothesis
may apply to simple rates, but it is difficult to even
start to comprehend what the null hypothesis
should be for traits such as colours, odours, morphology and so on. For this reason the empirical evidence
for active mate choice should be carefully re-examined
keeping in mind that the null hypothesis can vary
depending on the variation in the detectability of the
traits.
Above we argued that active mate choice can only be
inferred if we can demonstrate that there is a cost of
choice. Thus, even if we have the null hypothesis correct
and find that mating bias is more than expected by
chance, we still need to take the next step and determine
whether there exists a fitness cost for expressing the
choice. There are very few studies that have empirically
addressed the cost of mate choice (e.g. Milinski &
Bakker 1992; Wong & Jennions 2003; Byers et al. 2005;
for reviews see Gibson & Langen 1996; Jennions &
Petrie 1997). Most studies have concluded that choosiness decreases as costs of choice increases suggesting
that individuals may not be very willing to pay the
costs of mate choice (but see Byers et al. 2005). A
further complication in the interpretation of studies on
cost of mate choice is that the relevant currency at
which the cost should be measured is the reproductive
output of the female. Observing an energetic or time
cost of mating does not qualify as a cost of choice
unless it translates to reduced reproductive output (see
Kotiaho 2001 for similar argument for costs of expressing
sexual traits).
What is the magnitude of indirect benefits from
mate choice?
Recently, Kokko and others (2003) were astonished by
the fact that after two decades of intense empirical
work there still is no test of the fundamental prediction
of mate choice for indirect benefits, that is, that mate
choice will result in the increase in the net offspring
fitness. On a similar note, Fuller, Houle & Travis (2005)
proposed that empiricists should more rigorously test
whether male phenotype does indeed predict fitness
benefits. There are only a few studies that have measured
the benefits in terms of fitness (Boake 1985; Reynolds
& Gross 1992; Head et al. 2005; Qvarnström et al.
2006), although many more studies provide evidence
that mate choice may result in positive effects on some
fitness components of the offspring (e.g. Norris 1993;
Petrie 1994; Alatalo et al. 1998; Wedell & Tregenza
1999). Given that this has been a crucial aspect of
sexual selection based on indirect benefits for quite a
while, there are likely to be a number of studies that
may have attempted to find this effect. Moreover, given
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the likelihood of heavy publication bias towards
supportive evidence (Csada, James & Espie 1996; Kotiaho
& Tomkins 2002), it is surprising that in general the
magnitude of the indirect benefits from mate choice
are relatively small: a meta-analysis on viability
benefits showed that only about 1·5% of the variance in
offspring viability is explained by variance in preferred
male trait (Møller & Alatalo 1999). Given that most of
the studies included in the above meta-analysis have in
fact estimated the maximum potential benefit of
successful and accurate mate choice rather than the
realized benefit of actual mate choice, the benefits of
mate choice may be practically non-existent. Indeed, it
may be that the observed potential for benefits has
inadvertently led us to believe that this potential is also
realized, that is, that successful mate choice for indirect
benefits does occur.
Is it possible that active mate choice for indirect
benefits is just another anomaly created by
enthusiasm and publication bias?
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 638–644
To prevail in the ever-increasing competition in the
scientific enterprise, one needs to publish in highly
esteemed scientific journals. To publish a paper in such
a journal, it needs to have novel findings: lack of novelty
is an important rejection criterion. Novel findings are
given priority in publishing (as they often should be),
but when novelty and publishing become too important, we increase the risk of generating anomalies.
In fact, Kuhn (1996) described normal science as
‘... research firmly based upon one or more past
scientific achievements ...’, that ‘... does not aim at
novelties of fact or theory and, when successful, finds
none’. This description contrasts directly with today’s
publication policies. By aiming to publish novel papers
we may prevent the normal development of science.
Ironically, 10 years ago publishing scientists noted that
novelty is needed and increasingly started to use the
word ‘novel’ in the title or abstract of their publications
(Friedman & Karlsson 1997).
Another issue intimately related to novelty is the
issue of publishing non-significant results (Csada et al.
1996). When a study fails to find support for the
popular scientific idea, such as mate choice for indirect
benefits, it is easily dismissed as not sufficiently interesting to warrant publication. Moreover, it seems that
in order to get a non-significant main result published,
methodological and experimental rigor needs to be
extensively greater than when reporting significant
main results (see for example, Simmons et al. 1999;
Tomkins & Simmons 2003).
With the hunger for novelties, the tendency of not
writing up and publishing studies with non-significant
results and the more ready acceptance of supportive
studies working simultaneously, we will be more than
likely to generate extensive publication biases promoting
anomalies instead of true scientific discoveries. This is
proven by the fact that not only heritability of sexual
traits (Alatalo et al. 1997), but also many other popular scientific ideas in the field of evolutionary biology
have gone through a significant shift in the magnitude
of their effect in relation to the year of publication
(Gontard-Danek & Møller 1999; Møller & Alatalo
1999; Simmons et al. 1999; Jennions & Møller 2002;
Tomkins & Simmons 2003; see also Palmer 2000). The
explanation for such year-dependent effects is that in
the early phase of scientific discovery the enthusiasm
to find supportive results inevitably leads to publication bias; supportive studies get accepted more easily
resulting in an overestimate of the true effect size, but
as the discipline matures and scientific rigor settles in,
the estimates of the effect sizes shift closer to the true
effect sizes. There is a lesson to be learned: by aiming
at novel findings and allowing the publication bias to
exist, we may not be promoting science, but instead
may be hindering it. However, if we consciously
acknowledge the tendency of scientists to go astray by
jumping on the bandwagon, we should be able to avoid
these puzzling shifts in science.
Conclusions and directions for future research
In this paper we have argued that the evidence for
active mate choice for indirect benefits is not as
compelling as the current paradigm suggests, and that
the current emphasis on active mate choice for indirect
benefits has resulted in a distorted view of the nature
of sexual selection. For a better understanding of
evolution through sexual selection, it is of fundamental
importance to distinguish between the underlying
mechanisms generating biases in mating success:
active mate choice, passive attraction and male–male
competition. We emphasize that simply observing
mating bias, or even finding an indirect fitness benefit
of mating with a particular type of a male, can tell us
nothing about the underlying mechanisms generating
the mating bias. This is because all three mechanisms
can lead to identical indirect fitness benefits. Here we
suggest what we feel are three important areas that
require further study before active mate choice for
indirect fitness benefits should be concluded.
First, forming the null-hypothesis for mate choice
studies may be much more challenging than the common perception. Simply comparing the mating success
of males with varying trait size without taking into
account variation in the detectability of the trait is very
likely to lead to biased conclusions. For this reason the
empirical evidence for active mate choice should be
carefully re-examined keeping in mind that the null
hypothesis can vary depending on the variation in
the detectability of the traits. Deriving the correct
null-hypothesis may seem relatively easy for simple
rates, but it is much more difficult to comprehend
what the null hypothesis should be for traits such as
colours, odours, behaviours or morphology. What makes
things even more complicated is that, while the signal
itself often has some properties amenable to easy
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Ecological Society,
Functional Ecology,
21, 638–644
quantification, the detectability of the signal depends
also on the receiver. Unfortunately, what this means is
that simple mate choice experiments will often not be
able to tell whether some signals are more attractive
than others, or whether they are just more detectable.
What should be done is to determine whether detectability is a function of the signal, and when it is, this
function should be the null-hypothesis to test against
in the actual mate choice trials. We suspect, however,
that in practise deriving this function may prove to be
extremely difficult.
Second, the underlying mechanism generating the
mating bias must be shown to be active mate choice
rather than passive attraction or male–male competition. We suggest that this can only be done by directly
showing that females are willing to pay a cost for their
choice. The findings that experimentally increasing
the cost of performing mate choice leads to reduced
choosiness, already suggest that the costs that the
females are willing to pay from their choice may be
relatively small. The approach in which the cost is
manipulated and the choosiness observed is good and
we do need more studies like this. However, we propose
that future studies should also focus on devising ways
to manipulate female choice and observe the cost this
might introduce. When measuring the cost, however, it
is imperative to remember that the cost must be
measured in the relevant currency, that is, female
reproductive output: in theory, if it is experimentally
possible to prevent the choosy females from gaining the indirect genetic benefit from their choice, we
should see a reduction in female fitness (measured as
net offspring fitness) due to the cost of the choice.
Third, the magnitude of the indirect benefits related
to a particular male trait must be quantified. There
are many studies reporting benefits in some fitness
surrogates of the offspring, but only a handful that
have measured the benefit in the evolutionarily relevant
currency, the only relevant currency being the net
fitness of the offspring of the choosy female. Unfortunately, it is excessively laborious to obtain this estimate.
Nevertheless, to verify whether indirect benefits indeed
can play a role in mate choice, it is the direct net fitness
of the offspring of the choosy females, rather than
some fitness surrogates, that must be quantified. Even
after decades of research on the issue such studies
mostly do not exist, and our understanding of the
relevance of indirect benefits in mate choice remains
disgracefully poor. However, while we advocate the
measurement of indirect benefits in the relevant
currency, at the same time it must be kept in mind that
benefits can tell us nothing about the underlying
mechanisms generating the mating bias. This is because
all three mechanisms, active mate choice, passive
attraction and male–male competition can lead to
identical indirect fitness benefits. Therefore, each one
of the above three issues must be resolved before it can
be concluded that there is indeed evidence for active
mate choice for indirect fitness benefits.
Acknowledgements
We thank Rauno Alatalo and Heli Siitari for discussions and valuable comments to the manuscript. We
also thank two anonymous reviewers for helpful
comments. This work was supported by the Academy
of Finland and the Centre of Excellence in Evolutionary
Research.
References
Alatalo, R.V., Höglund, J. & Lundberg, A. (1991) Lekking in
the black grouse: a test of male viability. Nature 352, 155–156.
Alatalo, R.V., Kotiaho, J., Mappes, J. & Parri, S. (1998) Mate
choice for offspring performance: major benefits or minor
costs? Proceedings of the Royal Society of London B 265,
2297 – 2301.
Alatalo, R.V., Mappes, J. & Elgar, M.A. (1997) Heritabilities
and paradigm shifts. Nature 385, 402 – 403.
Andersson, M. (1982a) Female choice selects for extreme tail
length in a widowbird. Nature 299, 818 – 830.
Andersson, M. (1982b) Sexual selection, natural selection
and quality advertisement. Biological Journal of the Linnean
Society 17, 375 – 393.
Andersson, M. (1986a) Evolution of condition-dependent
sex ornaments and mating preferences: sexual selection
based on viability differences. Evolution 40, 804 –816.
Andersson, M. (1986b) Sexual selection and the importance
of viability differences: a reply. Journal of Theoretical
Biology 120, 251– 254.
Andersson, M. (1994) Sexual Selection. Princeton University
Press, Princeton.
Andersson, M. & Simmons, L.W. (2006) Sexual selection and
mate choice. Trends in Ecology and Evolution 21, 296–302.
Arak, A. (1988) Female mate selection in the natterjack toad:
active choice or passive attraction? Behavioral Ecology and
Sociobiology 22, 317 – 327.
Bateman, A.J. (1948) Intrasexual selection in Drosophila.
Heredity 2, 349 – 368.
Boake, C.R.B. (1985) Genetic consequences of mate choice:
a quantitative genetic method for testing sexual selection
theory. Science 227, 1061–1063.
Branham, M.A. & Greenfield, M.D. (1996) Flashing males
win mating success. Nature 381, 745 – 746.
Byers, J.A., Wiseman, P.A., Jones, L. & Roffe, T.J. (2005) A
large cost of female mate sampling in pronghorn. The
American Naturalist 166, 661– 668.
Castellano, S., Rosso, A. & Giacoma, C. (2004) Active
choice, passive attraction and the cognitive machinery of
acoustic preferences. Animal Behaviour 68, 323 –329.
Cronin, H. (1991) The Ant and the Peacock. Cambridge
University Press, Cambridge.
Csada, R.D., James, P.C. & Espie, R.H.M. (1996) The ‘file
drawer problem’ of non-significant results: does it apply to
biological research? Oikos 76, 591– 593.
Dall, S.R. et al. (2006) Debating sexual selection and mating
strategies. Science 312, 689 – 697.
Darwin, C. (1859) On the Origin of Species by Means of
Natural Selection. Murray, London.
Darwin, C.R. (1871) The Descent of Man and Selection in
Relation to Sex. John Murray, London.
Davis, J.W.F. & O’Donald, P. (1976) Sexual selection for a
handicap: a critical analysis of Zahavi’s model. Journal of
Theoretical Biology 57, 345 – 354.
Eshel, I., Volovik, I. & Sansone, E. (2000) On Fisher–Zahavi’s
handicapped sexy son. Evolutionary Ecology Research 2,
509 – 523.
Fisher, R.A. (1915) The evolution of sexual preference.
Eugenics Review 7, 184 –192.
643
Mate choice for
genetic benefits
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 638–644
Fisher, R.A. (1958) The Genetical Theory of Natural Selection.
Oxford University Press, Oxford.
Friedman, S.H. & Karlsson, J.O.M. (1997) A novel paradigm.
Nature 385, 480.
Fuller, R.C., Houle, D. & Travis, J. (2005) Sensory bias as an
explanation for the evolution of mate preferences. American
Naturalist 166, 437 – 446.
Gibson, R.M. & Langen, T.A. (1996) How do animals choose
their mates? Trends in Ecology and Evolution 11, 468 – 470.
Gontard-Danek, M.-C. & Møller, A.P. (1999) The strength of
sexual selection: a meta-analysis of bird studies. Behavioral
Ecology 10, 476 – 486.
Grafen, A. (1990) Biological signals as handicaps. Journal of
Theoretical Biology 144, 517 – 546.
Halliday, T.R. (1983) The study of mate choice. Mate Choice
(ed. P. Bateson), pp. 3 – 32. Cambridge University Press,
Cambridge.
Head, M.L., Hunt, J., Jennions, M.D. & Brooks, R. (2005)
The indirect benefits of mating with attractive males
outweigh the direct costs. PLoS Biology 3, e33.
Heisler, I.L. (1984) A quantitative genetic model for the
origin of mating preferences. Evolution 38, 1283 –1295.
Höglund, J. & Alatalo, R.V. (1995) Leks. Princeton University
Press, Princeton.
Houle, D. & Kondrashov, A.S. (2002) Coevolution of costly
mate choice and condition dependent display of good
genes. Proceedings of the Royal Society of London B,
Biological Sciences 269, 97 –104.
Huxley, J.S. (1938) The present standing of the theory of
sexual selection. Evolution: Essays on Aspects of Evolutionary
Biology (ed. G.R. De Beer), pp. 11– 41. Oxford University
Press, Oxford.
Iwasa, Y., Pomiankowski, A. & Nee, S. (1991) The evolution
of costly mate preferences II. The ‘handicap’ principle.
Evolution 45, 1431–1442.
Janetos, A.C. (1980) Strategies of female mate choice: a
theoretical analysis. Behavioral Ecology and Sociobiology
7, 107 –112.
Jennions, M.D. & Møller, A.P. (2002) Relationships fade with
time: a meta-analysis of temporal trends in publication in
ecology and evolution. Proceedings of the Royal Society of
London B, Biological Sciences 269, 43 – 48.
Jennions, M.D., Møller, A.P. & Petrie, M. (2001) Sexually
selected traits and adult survival: a meta-analysis.
Quarterly Review of Biology 76, 3 – 36.
Jennions, M.D. & Petrie, M. (1997) Variation in mate choice
and mating preferences: a review of causes and consequences.
Biological Reviews 72, 283 – 327.
Kirkpatrick, M. (1982) Sexual selection and the evolution of
female choice. Evolution 36, 1–12.
Kirkpatrick, M. & Ryan, M.J. (1991) The evolution of mating
preferences and the paradox of the lek. Nature 350, 33 – 38.
Kokko, H. (1998) Good genes, old age and life-history trade-offs.
Evolutionary Ecology 12, 739 – 750.
Kokko, H., Brooks, R., Jennions, M.D. & Morley, J. (2003)
The evolution of mate choice and mating biases. Proceedings
of the Royal Society of London B, Biological Sciences 270,
653 – 664.
Kokko, H., Brooks, R., McNamara, J.M. & Houston, A.I.
(2002) The sexual selection continuum. Proceedings of the
Royal Society of London B, Biological Sciences 269, 1331–
1340.
Kokko, H., Jennions, M.D. & Brooks, R. (2006) Unifying
and testing models of sexual selection. Annual Review of
Ecology, Evolution and Systematics 37, 43 – 66.
Kotiaho, J., Alatalo, R.V., Mappes, J. & Parri, S. (1996)
Sexual selection in a wolf spider: male drumming activity,
body size and viability. Evolution 50, 1977 –1981.
Kotiaho, J.S. (2001) Costs of sexual traits: a mismatch
between theoretical considerations and empirical evidence.
Biological Reviews 76, 365 – 376.
Kotiaho, J.S., Simmons, L.W. & Tomkins, J.L. (2001)
Towards a resolution of the lek paradox. Nature 410, 684–
686.
Kotiaho, J.S. & Tomkins, J.L. (2002) Meta-analysis can it ever
fail? Oikos 96, 551– 553.
Kuhn, T.S. (1996) The Structure of Scientific Revolutions. The
University of Chicago Press, Chicago.
Lande, R. (1981) Models of speciation by sexual selection on
polygenic traits. Proceedings of the National Academy of
Sciences of the United States of America 78, 3721–3725.
Maynard Smith, J. (1976) Sexual selection and the Handicap
principle. Journal of Theoretical Biology 57, 239–242.
Maynard Smith, J. (1985) Sexual selection, handicaps and
true fitness. Journal of Theoretical Biology 115, 1–8.
Maynard Smith, J. (1987) Sexual selection: a classification of
models. Sexual Selection: testing the alternatives (eds J.W.
Bradbury & M.B. Andersson), pp. 9–20. John Wiley &
Sons, Chichester.
Maynard Smith, J. (1991) Theories of sexual selection. Trends
in Ecology and Evolution 6, 146 –151.
Milinski, M. & Bakker, T.C.M. (1992) Costs influence
sequential mate choice in sticklebacks, Gasterosteus
aculeatus. Proceedings of the Royal Society of London B
250, 229 – 233.
Møller, A.P. & Alatalo, R.V. (1999) Good-genes effects in
sexual selection. Proceedings of the Royal Society of London
B 266, 85 – 91.
Norris, K. (1993) Heritable variation in a plumage indicator
of viability in male great tits Parus major. Nature 362, 537–
539.
O’Donald, P. (1980) Genetic Models of Sexual Selection.
Cambridge University Press, Cambridge.
Palmer, A.R. (2000) Quasi-replication and the contract of
error: lessons from sex rations, heritabilities and fluctuating
asymmetry. Annual Review of Ecology and Systematics 31,
441– 480.
Parker, G.A. (1979) Sexual selection and sexual conflict.
Sexual Selection and Reproductive Competition in Insects
(eds M.S. Blum & N. Blum), pp. 123 –166. Academic Press,
New York.
Parker, G.A. (1983) Mate quality and mating decisions. Mate
Choice (ed. P. Bateson), pp. 141–166. Cambridge University press, Cambridge.
Parri, S., Alatalo, R.V., Kotiaho, J. & Mappes, J. (1997)
Female choice for male drumming in the wolf spider
Hygrolycosa rubrofasciata. Animal Behaviour 53, 305–312.
Parri, S., Alatalo, R.V., Kotiaho, J.S., Mappes, J. & Rivero, A.
(2002) Sexual selection in the wolf spider Hygrolycosa
rubrofasciata: female preference for drum duration and
pulse rate. Behavioral Ecology, 13, 615– 621.
Petrie, M. (1994) Improved growth and survival of offspring of
peacocks with more elaborate trains. Nature 371, 598–599.
Pomiankowski, A. (1987) Sexual selection: the handicap
principle does work-sometimes. Proceedings of the Royal
Society of London B 231, 123 –145.
Pomiankowski, A., Iwasa, Y. & Nee, S. (1991) The evolution
of costly mate preferences I. Fisher and biased mutation.
Evolution 45, 1422 –1430.
Pomiankowski, A.N. (1988) The evolution of female mate
preferences for male genetic quality. Oxford Surveys in
Evolutionary Biology 5, 136 –184.
Qvarnström, A., Brommer, J.E. & Gustafsson, L. (2006)
Testing the genetics underlying the co-evolution of mate
choice and ornament in the wild. Nature 441, 84–86.
Reynolds, J.D. & Gross, M.R. (1992) Female mate preference
enhances offspring growth and reproduction in a fish,
Poecilia reticulata. Proceedings of the Royal Society of
London B, Biological Sciences 250, 57 – 62.
Roughgarden, J., Oishi, M. & Akcay, E. (2006) Reproductive
social behaviour: cooperative games to replace sexual
selection. Science 311, 965 – 969.
644
J. S. kotiaho &
M. Puurtinen
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Functional Ecology,
21, 638–644
Rowe, L. & Houle, D. (1996) The lek paradox and the capture
of genetic variance by condition dependent traits. Proceedings
of the Royal Society of London B 263, 1415 –1421.
Simmons, L.W., Tomkins, J.L., Kotiaho, J.S. & Hunt, J.
(1999) Fluctuating paradigm. Proceedings of the Royal
Society of London B 266, 593 – 595.
Tomkins, J.L., Radwan, J., Kotiaho, J.S. & Tregenza, T.
(2004) Genic capture and resolving the lek paradox. Trends
in Ecology and Evolution 19, 323 – 328.
Tomkins, J.L. & Simmons, L.W. (2003) Fluctuating asymmetry
and sexual selection: paradigm shifts, publication bias,
and observer expectation. Developmental Instability (ed.
M. Polak), pp. 231– 261. Oxford University Press, New
York.
Trivers, R.L. (1972) Parental investment and sexual selection.
Sexual Selection and the Descent of Man. 1871–1971 (ed. B.
Campbell), pp. 136 –172. Aldine-Atherton, Chicago.
Wagner, W.E.J. (1996) Convergent song preference between
female field crickets and acoustically orienting parasitoid
flies. Behavioral Ecology 7, 279 – 285.
Wallace, A.R. (1889) Darwinism. Murray, London.
Wedell, N. & Tregenza, T. (1999) Successful fathers sire
successful sons. Evolution 53, 620 – 625.
Williams, G.C. (1966) Adaptation and Natural Selection.
Princeton University Press, Princeton.
Wong, B.B.M. & Jennions, M.D. (2003) Costs influence male
mate choice in a freshwater fish. Proceedings of the Royal
Society of London B 270 (Suppl.), S36 – S38.
Zahavi, A. (1975) Mate selection: a selection for a handicap.
Journal of Theoretical Biology 53, 205 – 214.
Zahavi, A. (1977) The cost of honesty (further remarks on the
handicap principle). Journal of Theoretical Biology 67, 603–605.
Received 28 December 2006; revision 21 March 2007; accepted
12 April 2007
Editor: Duncan Irschick