The evolution of experience-mediated plasticity in mate preferences

Experience of sexual signals can alter mate preferences and influence the course of sexual selection. Here, we examine the patterns of experience-mediated plasticity in mate preferences that can arise in response to variation in the composition of mates in the environment. We use these patterns to test hypotheses about potential sources of selection favouring experience-mediated plasticity. We manipulated signal experience of female Enchenopa treehoppers (Hemiptera: Membracidae) in a vibrational playback experiment with the following treatments: silence; two types of non-preferred signals; preferred signals; and a mixture of preferred and non-preferred signals. This experiment revealed plasticity in mate preference selectivity, with greatest selectivity in the mixed signal treatment, followed by the preferred signal treatment. We found no plasticity in peak preference. These results suggest that females have been selected to adjust preference selectivity according to the variability of potential mates in their social environment, as well as to the presence/absence of preferred mates. We discuss how experience-mediated plasticity in mate preferences can influence the strength of selection on male signals and can result in evolutionary dynamics between variation in preferences and signals that either promote the maintenance of variation or facilitate rapid trait fixation.     

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.     

Experience-mediated plasticity in mate preferences: mating assurance in a variable environment

An individual's prior experience of sexual signals can result in variation in mate preferences, with important consequences for the course of sexual selection. We test two hypotheses about the evolution of experience-mediated plasticity in mate preferences: mating assurance and mismating avoidance. We exposed female Enchenopa binotata treehoppers (Hemiptera: Membracidae) to treatments that varied their experience of signal frequency, the most divergent sexual signal trait in the E. binotata species complex. Treatments consisted of (1) signals matching the preferred frequency, (2-3) signals deviating either 100 Hz above or 100 Hz below the preferred frequency, and (4) no signals. Females experiencing preferred signals showed the greatest selectivity. However, experience had no effect on peak preference. These results support the hypothesis that selection has favored plasticity in mate preferences that ensures that mating takes place when preferred mates are rare or absent, while ensuring choice of preferred types when those are present. We consider how experience-mediated plasticity may influence selection on sexual advertisement signals, patterns of reproductive isolation, and the maintenance of genetic variation. We suggest that the plasticity we describe may increase the likelihood of successful colonization of a novel environment, where preferred mating types may be rare.     

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.     

Stronger convex (stabilizing) selection on homologous sexual display traits in females than in males: a multipopulation comparison in Drosophila serrata

Mutual mate choice for homologous sexual display traits has been demonstrated in several recent studies yet little attention has been given to quantitative comparison of the strength and form of mate preferences between the sexes. Such comparisons may provide important insight into the evolution of mate choice for honest signals. In particular, because females generally provide the majority of resources for initial offspring development, female displays may trade-off with fecundity, causing preference evolution to differ between the sexes. Recent theory suggests that adaptive male preferences for honest displays in females are possible under certain conditions and may result in preferences that are convex (i.e., stabilizing) in form. We compared sexual selection on a suite of contact pheromones arising from mutual mate choice using nine separate geographic populations of Drosophila serrata. We show that the convex selection is stronger on females than on males overall in these populations, and that convex selection is the predominate form of nonlinear selection on females but not males.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies

Abstract Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle , divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle . However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.     

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.     

Signal reliability compromised by genotype-by-environment interaction and potential mechanisms for its preservation

Sexual selection based on signaling requires that signals used by females in mate choice are reliable indicators of a male's heritable total fitness. A signal and the preference for it are expected to be heritable, resulting in the maintenance of genetic covariance between these two traits. However, a recent article has proposed that signals may quickly become unreliable in the presence of both environmental variation and genotype-by-environment interaction (G x E) with crossing reaction norms, potentially compromising the mechanisms of sexual selection. Here we examine the heritability and plasticity of a male dominance advertisement in the bank vole, Clethrionomys glareolus, in stable and changing rearing environments from father to son. The bank vole is naturally exposed to considerable sources of spatial and temporal environmental variation and male reproductive success is determined by both intra- (male-male competition) and inter- (females prefer to mate with dominant males) sexual selection. Significant G x E for male dominance was found with crossing reaction norms. Plasma testosterone level (T), rather than condition, determined a male's dominance and T also showed a significant G x E. Dominance showed a considerable plasticity across environments, but was only heritable under stable conditions. We document a negative between-environments correlation of male dominance, suggesting that when the environment changes between father and son, the dominance signal is unreliable to females and sexual selection may be compromised. We discuss how G x E and environmental variation interacting with other mechanisms may preserve the reliability of signals and thus the mechanism of sexual selection itself.     

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.     

Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects

Mate choice is considered an important influence in the evolution of mating signals and other sexual traits, and--since divergence in sexual traits causes reproductive isolation--it can be an agent of population divergence. The importance of mate choice in signal evolution can be evaluated by comparing male signal traits with female preference functions, taking into account the shape and strength of preferences. Specifically, when preferences are closed (favouring intermediate values), there should be a correlation between the preferred values and the trait means, and stronger preferences should be associated with greater preference-signal correspondence and lower signal variability. When preferences are open (favouring extreme values), signal traits are not only expected to be more variable, but should also be shifted towards the preferred values. We tested the role of female preferences in signal evolution in the Enchenopa binotata species complex of treehoppers, a clade of plant-feeding insects hypothesized to have speciated in sympatry. We found the expected relationship between signals and preferences, implicating mate choice as an agent of signal evolution. Because differences in sexual communication systems lead to reproductive isolation, the factors that promote divergence in female preferences--and, consequently, in male signals--may have an important role in the process of speciation.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.     

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences

Sexual selection of high-quality mates can conflict with species recognition if traits that govern intraspecific mate preferences also influence interspecific recognition. This conflict might be resolved by developmental plasticity and learned mate preferences, which could drive preference divergence in populations that differ in local species composition. We integrate field and laboratory experiments on two calopterygid damselfly species with population genetic data to investigate how sex differences in developmental plasticity affect population divergence in the face of gene flow. Whereas male species recognition is fixed at emergence, females instead learn to recognize heterospecifics. Females are therefore more plastic in their mate preferences than males. We suggest that this results from sex differences in the balance between sexual selection for high-quality mates and selection for species recognition. As a result of these sex differences, females develop more pronounced population divergence in their mate preferences compared with males. Local ecological community context and presence of heterospecifics in combination with sex differences in plasticity and canalization therefore shape population divergence in mate preferences. As ongoing environmental change and habitat fragmentation bring formerly allopatric species into secondary contact, developmental plasticity of mate preferences in either or both sexes might facilitate coexistence and prevent local species extinction.     

Cuticular hydrocarbons influence female attractiveness to males in the Australian field cricket,Teleogryllus oceanicus

Sexual dimorphism is thought to result from directional sexual selection acting on male signal traits, with female signal traits given little, if any, attention. Here, we examine male mating preferences in the Australian field cricket, Teleogryllus oceanicus. Using a multivariate selection analysis approach, we found that male preferences have the potential to exert selection on female cuticular hydrocarbons, chemical compounds widely used as sexual signals in insects. In addition to finding both stabilizing and disruptive preference gradients, we also found weak negative directional preference for female cuticular hydrocarbons. We contrast our results with a recent study examining sexual selection via female choice on male T. oceanicus cuticular hydrocarbons and suggest that differences in the form and intensity of sexual selection between the genders may provide part of the net selection differential necessary for the evolution of sexual dimorphism in this species.     

Sexual selection on Drosophila serrata male pheromones does not vary with female age or mating status

Mate preferences are costly and are thought to evolve due to the direct and/or indirect benefits they provide. Such costs and benefits may vary in response to intrinsic and extrinsic factors with important evolutionary consequences. Limited attention has been given to quantifying such variation and understanding its causes, most notably with respect to the direction and strength of preferences for multivariate sexual displays. In Drosophila serrata, female preferences target a pheromone blend of long‐chain cuticular hydrocarbons (CHCs). We used a factorial design to test whether female age and mating status generated variation in the strength and direction of sexual selection on male CHCs. Replicate choice mating trials were conducted using young and old females (4 or 10 days post‐emergence) that were either virgin or previously mated. The outcome of such trials is known to capture variation in female mate preferences, although male–male interactions may also contribute. Directional sexual selection on male CHCs was highly significant within each treatment, but there was little evidence of any variation among treatments. The absence of treatment effects implies that the multivariate combination of male CHCs preferred by females was constant with respect to female age and mating status. To the extent that male–male interactions may also contribute, our results similarly imply that these did not vary among treatments groups. With respect to D. serrata mate preferences, our results suggest that either plasticity with respect to age and mating status is not beneficial to females, or preference expression is somehow constrained.     

Genotype-by-Environment Interactions for Female Mate Choice of Male Cuticular Hydrocarbons in Drosophila simulans

Recent research has highlighted the potential importance of environmental and genotype-by-environment (G×E) variation in sexual selection, but most studies have focussed on the expression of male sexual traits. Consequently, our understanding of genetic variation for plasticity in female mate choice is extremely poor. In this study we examine the genetics of female mate choice in Drosophila simulans using isolines reared across two post-eclosion temperatures. There was evidence for G×Es in female choosiness and preference, which suggests that the evolution of female mate choice behaviour could differ across environments. However, the ranked order of preferred males was consistent across females and environments, so the same males are favoured by mate choice in spite of G×Es. Our study highlights the importance of taking cross-environment perspectives in order to gain a more comprehensive understanding of the operation of sexual selection.     

The Evolutionary Consequences of Disrupted Male Mating Signals: An Agent-Based Modelling Exploration of Endocrine Disrupting Chemicals in the Guppy

Females may select a mate based on signalling traits that are believed to accurately correlate with heritable aspects of male quality. Anthropogenic actions, in particular chemicals released into the environment, are now disrupting the accuracy of mating signals to convey information about male quality. The long-term prediction for disrupted mating signals is most commonly loss of female preference. Yet, this prediction has rarely been tested using quantitative models. We use agent-based models to explore the effects of rapid disruption of mating signals. In our model, a gene determines survival. Males signal their level of genetic quality via a signal trait, which females use to select a mate. We allowed this system of sexual selection to become established, before introducing a disruption between the male signal trait and quality, which was similar in nature to that induced by exogenous chemicals. Finally, we assessed the capacity of the system to recover from this disruption. We found that within a relatively short time frame, disruption of mating signals led to a lasting loss of female preference. Decreases in mean viability at the population-level were also observed, because sexual-selection acting against newly arising deleterious mutations was relaxed. The ability of the population to recover from disrupted mating signals was strongly influenced by the mechanisms that promoted or maintained genetic diversity in traits under sexual selection. Our simple model demonstrates that environmental perturbations to the accuracy of male mating signals can result in a long-term loss of female preference for those signals within a few generations. What is more, the loss of this preference can have knock-on consequences for mean population fitness.     

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.     

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.