Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection

Variation among females in mate choice may influence evolution by sexual selection. The genetic basis of this variation is of interest because the elaboration of mating preferences requires additive genetic variation in these traits. Here we measure the repeatability and heritability of two components of female choosiness (responsiveness and discrimination) and of female preference functions for the multiple ornaments borne by male guppies (Poecilia reticulata). We show that there is significant repeatable variation in both components of choosiness and in some preference functions but not in others. There appear to be several male ornaments that females find uniformly attractive and others for which females differ in preference. One consequence is that there is no universally attractive male phenotype. Only responsiveness shows significant additive genetic variation. Variation in responsiveness appears to mask variation in discrimination and some preference functions and may be the most biologically relevant source of phenotypic and genetic variation in mate-choice behavior. To test the potential evolutionary importance of the phenotypic variation in mate choice that we report, we estimated the opportunity for and the intensity of sexual selection under models of mate choice that excluded and that incorporated individual female variation. We then compared these estimates with estimates based on measured mating success. Incorporating individual variation in mate choice generally did not predict the outcome of sexual selection any better than models that ignored such variation.     

Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.     

Describing mate preference functions and other function‐valued traits

Mate preferences are important causes of sexual selection. They shape the evolution of sexual ornaments and displays, sometimes maintaining genetic diversity and sometimes promoting speciation. Mate preferences can be challenging to study because they are expressed in animal brains and because they are a function of the features of potential mates that are encountered. Describing them requires taking this into account. We present a method for describing and analysing mate preference functions, and introduce a freely available computer program that implements the method. We give an overview of how the program works, and we discuss how it can be used to visualize and quantitatively analyse preference functions. In addition, we provide an informal review of different methods of testing mate preferences, with recommendations for how best to set up experiments on mate preferences. Although the program was written with mate preferences in mind, it can be used to study any function‐valued trait, and we hope researchers will take advantage of it across a broad range of traits.     

Fluctuating mate preferences in a marine fish

According to theory, directional female choice for male sexual ornaments is expected to erode underlying genetic variation. Considerable attention, in this regard, has been given to understanding the ubiquity of heritable genetic variation in both female choice and male sexual traits. One intriguing possibility emerging from this work is that persistent genetic variation could be maintained, over time, by variation in female mate preferences. Here, we report the results of a four-year study showing significant year-to-year fluctuations in mate preferences in a small marine fish, the sand goby, Pomatoschistus minutus. Although the average size of mature fish varied across years, we were unable to find direct evidence linking this variation to differences in female preferences among years. Our results, nevertheless, underscore the importance of temporal fluctuations in female mate preferences, as these can have important consequences for understanding variation in sexual traits and the intensity of sexual selection.     

The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype‐linked fertility hypothesis

The origin and maintenance of mating preferences continues to be an important and controversial topic in sexual selection research. Leks and lek‐like mating systems, where individuals gather in particular spots for the sole purpose of mate choice, are particularly puzzling, because the strong directional selection imposed by mate choice should erode genetic variation among competing individuals and negate any benefit for the choosing sex. Here, we take advantage of the lek‐like mating system of the worm pipefish (Nerophis lumbriciformis) to test the phenotype‐linked fertility hypothesis for the maintenance of mating preferences. We use microsatellite markers to perform a parentage analysis, along with a mark–recapture study, to confirm that the worm pipefish has an unusual mating system that strongly resembles a female lek, where females display and males visit the lek to choose mates. Our results show that the most highly ornamented females occupy positions near the centre of the breeding area, and males mating with these females receive fuller broods with larger eggs compared to males mating with less‐ornamented females. We also conduct a laboratory experiment to show that female ornaments are condition‐dependent and honestly signal reproductive potential. Overall, these results are consistent with the predictions of a sex‐independent version of the phenotype‐linked fertility hypothesis, as male preference for female ornaments correlates with fertility benefits.     

Local population density and group composition influence the signal‐preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae)

Many animals exhibit social plasticity – changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences – the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant‐feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density – favouring higher signal frequencies in denser environments. Thus, local density changes the signal–preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal–preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Variation in preference for a male ornament is positively associated with female eyespan in the stalk-eyed fly Diasemopsis meigenii

There is currently much interest in mate preferences for sexual ornaments. However, few studies have focused on individual variation in mate preference despite its importance for the rate and direction of sexual selection. Females of the sexually dimorphic stalk-eyed fly, Diasemopsis meigenii, exhibit an unambiguous rejection response towards unattractive males bearing small ornaments. We investigated individual mate preferences using repeated sequential sampling of female rejection or acceptance responses to a wide range of male ornament phenotypes. We found significant variation in the strength of individual preference. In addition, preference was positively associated with female eyespan, a condition-dependent trait putatively linked to visual acuity.     

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae)

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full‐sibling, split‐family rearing design to estimate genetic correlations (r_G) between fecundity and signal traits, and compared those relationships against population‐level mate preferences for the signal traits. Animal model estimates for r_G between female fecundity and male signal traits overlapped zero—rejecting the hypothesis—but could reflect sample size limitations. The magnitude of r_G correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population‐level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high‐performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.     

THE EVOLUTION OF MATE PREFERENCES FOR MULTIPLE SEXUAL ORNAMENTS

Males of many species use multiple sexual ornaments in their courtship display. We investigate the evolution of female sexual preferences for more than a single male trait by the handicap process. The handicap process assumes that ornaments are indicators of male quality, and a female benefits from mate choice by her offspring inheriting “good genes” that increase survival chances. A new handicap model is developed that allows equilibria to be given in terms of selection pressures, independent of genetic parameters. Multiple sexual preferences evolve if the overall cost of choice is not greatly increased by a female using additional male traits in her assessment of potential mates. However, only a single preference is evolutionarily stable if assessment of additional male traits greatly increases the overall cost of choice (more than expected by combining the cost of each preference independently). Any single preference can evolve, the outcome being determined by initial conditions. The evolution of one preference effectively blocks the evolution of others, even for traits that are better indicators of male quality. Comparison is made with sexual selection caused by Fisher's runaway process in which male traits are purely attractive characters. This shows that sexual preferences for multiple Fisher traits are likely to evolve alongside preference for a single handicap trait that indicates male quality. This is a general difference in the evolutionary outcome of these two causes of sexual selection.     

Variation in female mate choice within guppy populations: population divergence,multiple ornaments and the maintenance of polymorphism

The evolutionary significance of variation in mate choice behaviour is currently a subject of some debate and considerable empirical study. Here, I review recent work on variation within and among guppy (Poecilia reticulata) populations in female mate choice and mating preferences. Empirical results demonstrate that there is substantial variation within and among populations in female responsiveness and choosiness, and much of this variation is genetic. Evidence for variation in preference functions also exists, but this appears to be more equivocal and the relative importance of genetic variation is less clear cut. In the second half of this review I discuss the potential significance of this variation to three important evolutionary issues: the presence of multiple male ornaments, the maintenance of polymorphism and divergence in mate recognition among populations. Studies of genetic variation in mate choice within populations indicate that females have complex, multivariate preferences that are able to evolve independently to some extent. These findings suggest that the presence of multiple male ornaments may be due to multiple female mating preferences. The extreme polymorphism in male guppy colour patterns demands explanation, yet no single satisfactory explanation has yet emerged. I review several old ideas and a few new ones in order to identify the most promising potential explanations for future empirical testing. Among these are negative frequency dependent selection, environmental heterogeneity coupled with gene flow, and genetic constraints. Last, I review the relative extent of within and among-population variation in mate choice and mating preferences in order to assess why guppies have not speciated despite a history of isolation and divergence. I argue that variation within guppy populations in mate choice and enhanced mating success of new immigrants to a pool are major impediments to population divergence of the magnitude that would be required for speciation to occur.     

QUANTITATIVE GENETICS OF FEMALE MATE PREFERENCES IN AN ANCESTRAL AND A NOVEL ENVIRONMENT

A female's mate preference is a potentially complex function relating variation in multiple male phenotypes with her probability of accepting individual males as a mate. Estimating the quantitative genetic basis preference functions within a population is empirically challenging yet key to understanding preference evolution. We employed a recently described approach that uses random‐coefficient mixed models in the analysis of function‐valued traits. Using a half‐sibling breeding design in a laboratory‐adapted Drosophila serrata population, we estimated the genetic (co)variance function of female preference for male sexual displays composed of nine contact pheromones. The breeding design was performed across two environments: the food to which the population was well adapted and a novel food that reduced average female productivity by 35%. Significant genetic variance in female preference was detected and the majority (64.2%) was attributable to a single genetic dimension (eigenfunction), suggesting that preferences for different pheromones are not genetically independent. The second eigenfunction, accounting for 24% of the total genetic variance, approached significance in a conservative test, suggesting the existence of a second, independent genetic dimension. There was no evidence that the genetic basis of female preference differed between the two environments, suggesting the absence of genotype‐by‐environment interactions and hence a lack of condition‐dependent preference expression.     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Genotype‐by‐environment interactions for cuticular hydrocarbon expression in Drosophila simulans

Genotype‐by‐environment interactions (G × Es) describe genetic variation for phenotypic plasticity. Recent interest in the role of these interactions in sexual selection has identified G × Es across a diverse range of species and sexual traits. Additionally, theoretical work predicts that G × Es in sexual traits could help to maintain genetic variation, but could also disrupt the reliability of these traits as signals of mate quality. However, empirical tests of these theoretical predictions are scarce. We reared iso‐female lines of Drosophila simulans across two axes of environmental variation (diet and temperature) in a fully factorial design and tested for G × Es in the expression of cuticular hydrocarbons (CHCs), a multivariate sexual trait in this species. We find sex‐specific environmental, genetic and G × E effects on CHC expression, with G × Es for diet in both male and female CHC profile and a G × E for temperature in females. We also find some evidence for ecological crossover in these G × Es, and by quantifying variance components, genetic correlations and heritabilities, we show the potential for these G × Es to help maintain genetic variation and cause sexual signal unreliability in D. simulans CHC profiles.     

Evolution of a mating preference for a dual‐utility trait used in intrasexual competition in genetically monogamous populations

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.     

Sexual selection and condition-dependent mate preferences

The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.     

Patterns of fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

Reproductive character displacement of female mate preferences for male cuticular hydrocarbons in Drosophila subquinaria

Several lines of evidence implicate sexual isolation in both initiating and completing the speciation process. Although its existence is straightforward to demonstrate, understanding the evolution of sexual isolation requires identifying the underlying phenotypes responsible so that we can determine how these have diverged. Here, we study geographic variation in female mate preferences for male sexual displays in the fly Drosophila subquinaria. Female D. subquinaria that are sympatric with its sister species D. recens discriminate strongly against both D. recens and allopatric conspecific males, whereas females from allopatric populations do not. Furthermore, female mate preferences target at least in part a suite of cuticular hydrocarbons (CHCs) in males and geographic variation in CHCs mirrors the pattern of mate discrimination. In this study, we quantify female mate preferences for male CHCs from populations that span the geographic range of D. subquinaria. We find that the direction of linear sexual selection varies significantly between populations that are sympatric versus allopatric with D. recens in a pattern of reproductive character displacement. Differences in preference partially align with existing differences in CHCs and patterns of sexual isolation, although discrepancies remain that suggest the involvement of additional traits and/or more complex, nonlinear preference functions.     

Phenotypic plasticity in female mate choice behavior is mediated by an interaction of direct and indirect genetic effects in Drosophila melanogaster

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.     

The effects of sexual selection on trait divergence in a peripheral population with gene flow

The unique aspects of speciation and divergence in peripheral populations have long sparked much research. Unidirectional migration, received by some peripheral populations, can hinder the evolution of distinct differences from their founding populations. Here, we explore the effects that sexual selection, long hypothesized to drive the divergence of distinct traits used in mate choice, can play in the evolution of such traits in a partially isolated peripheral population. Using population genetic continent‐island models, we show that with phenotype matching, sexual selection increases the frequency of an island‐specific mating trait only when female preferences are of intermediate strength. We identify regions of preference strength for which sexual selection can instead cause an island‐specific trait to be lost, even when it would have otherwise been maintained at migration‐selection balance. When there are instead separate preference and trait loci, we find that sexual selection can lead to low trait frequencies or trait loss when female preferences are weak to intermediate, but that sexual selection can increase trait frequencies when preferences are strong. We also show that novel preference strengths almost universally cannot increase, under either mating mechanism, precluding the evolution of premating isolation in peripheral populations at the early stages of species divergence.