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.     

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.     

Quantitative genetic models of sexual selection

Modeling of R.A. Fisher's ideas about the evolution of male ornamentation using quantitative genetics began in the 1980s. Following an initial period of enthusiasm, interest in these models began to wane when theoretical studies seemed to show that the rapid evolution of ornaments would not occur if there were costs associated with female mate choice. Recent theoretical work has shown, however, that runaway evolution and other kinds of extensive diversification of ornaments and preferences can occur, even when female choice is costly. These new models highlight crucial parameters that profoundly influence evolutionary trajectories, but these parameters have been neglected in empirical studies. Here, we review quantitative genetic models of sexual selection with the aim of fostering communication and synergism between theoretical and empirical enterprises. We also point out several areas in which additional empirical work could distinguish between alternative models of evolution.     

Eyespan reflects reproductive quality in wild stalk-eyed flies

Handicap models of sexual selection propose that females use male sexual ornaments as a cue in mate choice because they reflect commodities that increase female fitness, either directly or indirectly. In contrast to studies on vertebrates, most investigations of ornaments in insects and other invertebrate taxa have been conducted under laboratory conditions. There is a pressing need to address questions relating to sexual signalling of quality in natural populations, as the arbitrary and uniform environments found in the laboratory fail to reflect the world under which animals have evolved. We investigated associations between male ornaments (exaggerated eyespan), attractiveness, and reproductive quality in a wild population of the sexually ornamented stalk-eyed fly, Teleopsis dalmanni. We also explored the relationship between eyespan and reproductive quality in females to evaluate the potential for sexually antagonistic selection on eyespan. We show that eyespan is a generic correlate of reproductive quality, acting as a reliable mirror of variation in reproductive fitness in both sexes. Our findings suggest that male ornaments signal commodities that are of interest to females in the natural environment in which they, and mate preferences for them, have evolved. In addition, the covariance between female eyespan and reproductive output suggests that the former may be a reliable cue of quality in its own right. Our data provide important insights into the evolutionary forces that shape the evolution of exaggerated eyespan in wild populations of this species.     

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as ‘Fisherian runaway’. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.     

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.     

The evolution of female preferences for multiple indicators of quality

In a variety of species, females exhibit preferences for multiple male ornaments. Several hypotheses have been proposed to explain this phenomenon. Which, if any, of these hypotheses is the most plausible in general remains largely unresolved based on the available empirical data. Yet theoretical studies conclude that the evolution of preferences for multiple signals of male quality is unlikely, especially when the use of an additional cue in mate choice strongly increases the overall cost of choice. This would imply that most male courtship characters do not reflect the male's genetic quality but instead evolved through Fisherian sexual selection. However, the existing models focus on ornaments that signal overall genetic quality and do not address the possibility that different ornaments provide information about different aspects of quality. Therefore, we develop a model in which the ornaments act as signals for distinct quality components. When the ornaments provide overlapping information about these quality components, we retrieve the results of earlier models. However, when the ornaments provide independent information, preferences for multiple ornaments may evolve, even when exhibiting multiple preferences is costly. We discuss our results in relation to the multiple-message and redundant-signal hypotheses for ornament diversity and identify parallels between Fisherian and good-genes mechanisms for the evolution of multiple ornaments.     

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.     

Male mate choice,male quality,and the potential for sexual selection on female traits under polygyny

Observations of male mate choice are increasingly common, even in species with traditional sex roles. In addition, female traits that bear the hallmarks of secondary sexual characters are increasingly reported. These concurrent empirical trends have led to the repeated inference that, even under polygyny, male mate choice is a mechanism of sexual selection on female traits. It is often either assumed or argued that in these cases females are competing for males of superior “quality”; females might experience sexual selection under polygyny if they compete for mates that provide either direct or indirect benefits. However, the theoretical foundation of this testable hypothesis remains largely uninvestigated. We develop a population genetic model to probe the logic of this hypothesis and demonstrate that, contrary to common inferences, male mate choice, variation in male quality (in the form of a direct fecundity benefit to females), and female ornamentation can coexist in a population without any sexual selection on female ornamentation taking place at all. Furthermore, even in a “best case scenario” where high quality males with a preference for ornamented females are able to mate disproportionately more often with them, the evolution of female traits by sexual selection may be relatively weak. We discuss the implication of these findings for ongoing empirical and theoretical research on the evolution of sexual‐signaling in females.     

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.     

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

Comparing complex fitness surfaces: among-population variation in mutual sexual selection in Drosophila serrata

Despite a dramatic increase in empirical estimates of phenotypic selection over the past two decades, we remain remarkably ignorant about variation in the multivariate fitness surfaces that shape the adaptive landscape. We develop a novel approach for quantifying patterns of spatial and/or temporal variation in multivariate selection that directly compares vectors of linear selection gradients (beta) and matrices of nonlinear selection gradients (gamma) that describe the multivariate fitness surface in each population. We apply this approach to estimates of sexual selection on a suite of cuticular hydrocarbons (CHCs) in males and females from nine geographic populations of Drosophila serrata. In males, variation in linear sexual selection was associated with the presence of the related species Drosophila birchii, suggesting that female mate preferences for male CHCs differ between sympatry and allopatry. This is consistent with previous experimental results suggesting that reproductive character displacement of male CHCs has resulted from selection caused by the presence of D. birchii. No significant associations were found for nonlinear sexual selection in males. In females, large-scale variation in both linear and nonlinear sexual selection was negatively associated with assumed-neutral population genetic structure, suggesting a key role for chance events in male mate preference divergence.     

Parasite levels in blue-black grassquits correlate with male displays but not female mate preference

The handicap principle proposes that male sexual ornaments anddisplays provide honest indicators of quality. Female preferencefor high-quality males, however, may be driven not only by geneticbenefits but also by indirect benefits. We investigated theimpact of parasitism on morphological, ornamental, and behavioralcharacteristics of male and female blue-black grassquits (Volatiniajacarina) in captivity. First, we tested whether male displaysand morphology were influenced by parasitism. Second, we assessedif females were attentive to variation in male morphology anddisplays linked to parasitism. Third, we tested whether parasitismin females influenced health and mate preferences. We maintained2 groups of birds in captivity: nonmedicated birds developedhigh levels of coccidian parasitism, whereas medicated birdswere free of parasitism. Parasitized males developed, relativeto nonparasitized males, lower weight/tarsus indices and mass.They also showed relative deficiencies in their displays, withless persistence and lower rates. Despite the negative effectsof parasitism on males, females did not prefer nonparasitizedmales. This held for both parasitized and nonparasitized females.Our data suggest that coccidian parasitism has adverse effectson morphological condition and expression of displays. Theseeffects, however, appear not to be attended to by females; moreover,female mate preferences appear not to be impacted by the threatof parasitism. It thus seems that female mate preferences maynot depend only on sexual characters affected by parasitismin this species.     

Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua)

Little evidence of benefits from female mate choice has been found when males provide no parental care or resources. Yet, good genes models of sexual selection suggest that elaborated male sexual characters are reliable signals of mate quality and that the offspring of males with elaborate sexual ornaments will perform better than those of males with less elaborate ornaments. We used cod (Gadus morhua L.), an externally fertilizing species where males provide nothing but sperm, to examine the potential of optimal mate selection with respect to offspring survival. By applying in vitro fertilizations, we crossed eight females with nine males in all possible combinations and reared each of the 72 sib groups. We found that offspring survival was dependent on which female was mated with which male and that optimal mate selection has the potential to increase mean offspring survival from 31.9 to 55.6% (a 74% increase). However, the size of the male sexual ornaments and sperm quality (i.e. sperm velocity and sperm density) could not predict offspring survival. Thus, even if there may be large fitness benefits of mate selection, we might not yet have identified the male characteristics generating high offspring survival.     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

Can non‐directional male mating preferences facilitate honest female ornamentation?

Recent studies have demonstrated male mate choice for female ornaments in species without sex-role reversal. Despite these empirical findings, little is known about the adaptive dynamics of female signalling, in particular the evolution of male mating preferences. The evolution of traits that signal mate quality is more complex in females than in males because females usually provide the bulk of resources for the developing offspring. Here, we investigate the evolution of male mating preferences using a mathematical model which: (i) specifically accounts for the fact that females must trade-off resources invested in ornaments with reproduction; and (ii) allows male mating preferences to evolve a non-directional shape. The optimal adaptive strategy for males is to develop stabilizing mating preferences for female display traits to avoid females that either invests too many or too few resources in ornamentation. However, the evolutionary stability of this prediction is dependent upon the level of error made by females when allocating resources to either signal or fecundity.     

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.     

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to tradition explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side-effect of females evolving to reduce the direct costs of mating.