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

Transcription

1 Functional Ecology 2007 Blackwell Publishing Ltd ESSARY REVIEW 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, University of Jyväskylä, Finland, Natural History Museum, P. O. Box 35, 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) doi: /j x 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. janne.kotiaho@bytl.fi 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, 638

2 639 Mate choice for genetic benefits 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

3 640 J. S. kotiaho & M. Puurtinen 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 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

4 641 Mate choice for genetic benefits 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? 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

5 642 J. S. kotiaho & M. Puurtinen 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, 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, Alatalo, R.V., Mappes, J. & Elgar, M.A. (1997) Heritabilities and paradigm shifts. Nature 385, Andersson, M. (1982a) Female choice selects for extreme tail length in a widowbird. Nature 299, Andersson, M. (1982b) Sexual selection, natural selection and quality advertisement. Biological Journal of the Linnean Society 17, Andersson, M. (1986a) Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40, Andersson, M. (1986b) Sexual selection and the importance of viability differences: a reply. Journal of Theoretical Biology 120, 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, Arak, A. (1988) Female mate selection in the natterjack toad: active choice or passive attraction? Behavioral Ecology and Sociobiology 22, Bateman, A.J. (1948) Intrasexual selection in Drosophila. Heredity 2, Boake, C.R.B. (1985) Genetic consequences of mate choice: a quantitative genetic method for testing sexual selection theory. Science 227, Branham, M.A. & Greenfield, M.D. (1996) Flashing males win mating success. Nature 381, 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, Castellano, S., Rosso, A. & Giacoma, C. (2004) Active choice, passive attraction and the cognitive machinery of acoustic preferences. Animal Behaviour 68, 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, Dall, S.R. et al. (2006) Debating sexual selection and mating strategies. Science 312, 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, Eshel, I., Volovik, I. & Sansone, E. (2000) On Fisher Zahavi s handicapped sexy son. Evolutionary Ecology Research 2, Fisher, R.A. (1915) The evolution of sexual preference. Eugenics Review 7,

6 643 Mate choice for genetic benefits 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, Gibson, R.M. & Langen, T.A. (1996) How do animals choose their mates? Trends in Ecology and Evolution 11, Gontard-Danek, M.-C. & Møller, A.P. (1999) The strength of sexual selection: a meta-analysis of bird studies. Behavioral Ecology 10, Grafen, A. (1990) Biological signals as handicaps. Journal of Theoretical Biology 144, Halliday, T.R. (1983) The study of mate choice. Mate Choice (ed. P. Bateson), pp 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, 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, 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 Oxford University Press, Oxford. Iwasa, Y., Pomiankowski, A. & Nee, S. (1991) The evolution of costly mate preferences II. The handicap principle. Evolution 45, Janetos, A.C. (1980) Strategies of female mate choice: a theoretical analysis. Behavioral Ecology and Sociobiology 7, 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, Jennions, M.D., Møller, A.P. & Petrie, M. (2001) Sexually selected traits and adult survival: a meta-analysis. Quarterly Review of Biology 76, Jennions, M.D. & Petrie, M. (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews 72, Kirkpatrick, M. (1982) Sexual selection and the evolution of female choice. Evolution 36, Kirkpatrick, M. & Ryan, M.J. (1991) The evolution of mating preferences and the paradox of the lek. Nature 350, Kokko, H. (1998) Good genes, old age and life-history trade-offs. Evolutionary Ecology 12, 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, 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, Kokko, H., Jennions, M.D. & Brooks, R. (2006) Unifying and testing models of sexual selection. Annual Review of Ecology, Evolution and Systematics 37, 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, Kotiaho, J.S. (2001) Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biological Reviews 76, Kotiaho, J.S., Simmons, L.W. & Tomkins, J.L. (2001) Towards a resolution of the lek paradox. Nature 410, Kotiaho, J.S. & Tomkins, J.L. (2002) Meta-analysis can it ever fail? Oikos 96, 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, Maynard Smith, J. (1976) Sexual selection and the Handicap principle. Journal of Theoretical Biology 57, 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 John Wiley & Sons, Chichester. Maynard Smith, J. (1991) Theories of sexual selection. Trends in Ecology and Evolution 6, 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, Møller, A.P. & Alatalo, R.V. (1999) Good-genes effects in sexual selection. Proceedings of the Royal Society of London B 266, Norris, K. (1993) Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362, 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, Parker, G.A. (1979) Sexual selection and sexual conflict. Sexual Selection and Reproductive Competition in Insects (eds M.S. Blum & N. Blum), pp Academic Press, New York. Parker, G.A. (1983) Mate quality and mating decisions. Mate Choice (ed. P. Bateson), pp 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, 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, Petrie, M. (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371, Pomiankowski, A. (1987) Sexual selection: the handicap principle does work-sometimes. Proceedings of the Royal Society of London B 231, Pomiankowski, A., Iwasa, Y. & Nee, S. (1991) The evolution of costly mate preferences I. Fisher and biased mutation. Evolution 45, Pomiankowski, A.N. (1988) The evolution of female mate preferences for male genetic quality. Oxford Surveys in Evolutionary Biology 5, 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, 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, Roughgarden, J., Oishi, M. & Akcay, E. (2006) Reproductive social behaviour: cooperative games to replace sexual selection. Science 311,

7 644 J. S. kotiaho & M. Puurtinen 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, Simmons, L.W., Tomkins, J.L., Kotiaho, J.S. & Hunt, J. (1999) Fluctuating paradigm. Proceedings of the Royal Society of London B 266, Tomkins, J.L., Radwan, J., Kotiaho, J.S. & Tregenza, T. (2004) Genic capture and resolving the lek paradox. Trends in Ecology and Evolution 19, 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 Oxford University Press, New York. Trivers, R.L. (1972) Parental investment and sexual selection. Sexual Selection and the Descent of Man (ed. B. Campbell), pp Aldine-Atherton, Chicago. Wagner, W.E.J. (1996) Convergent song preference between female field crickets and acoustically orienting parasitoid flies. Behavioral Ecology 7, Wallace, A.R. (1889) Darwinism. Murray, London. Wedell, N. & Tregenza, T. (1999) Successful fathers sire successful sons. Evolution 53, 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, Zahavi, A. (1977) The cost of honesty (further remarks on the handicap principle). Journal of Theoretical Biology 67, Received 28 December 2006; revision 21 March 2007; accepted 12 April 2007 Editor: Duncan Irschick