Mate choice for genetic quality when environments vary: suggestions for empirical progress

Mate choice for good-genes remains one of the most controversial evolutionary processes ever proposed. This is partly because strong directional choice should theoretically deplete the genetic variation that explains the evolution of this type of female mating preference (the so-called lek paradox). Moreover, good-genes benefits are generally assumed to be too small to outweigh opposing direct selection on females. Here, we review recent progress in the study of mate choice for genetic quality, focussing particularly on the potential for genotype by environment interactions (GEIs) to rescue additive genetic variation for quality, and thereby resolve the lek paradox. We raise five questions that we think will stimulate empirical progress in this field, and suggest directions for research in each area: (1) How is condition-dependence affected by environmental variation? (2) How important are GEIs for maintaining additive genetic variance in condition? (3) How much do GEIs reduce the signalling value of male condition? (4) How does GEI affect the multivariate version of the lek paradox? (5) Have mating biases for high-condition males evolved because of indirect benefits?     

Genetic variance of sexually selected traits in waxmoths: maintenance by genotype x environment interaction

When traits experience directional selection, such as that imposed by sexual selection, their genetic variance is expected to diminish. Nonetheless, theory and findings from sexual selection predict and demonstrate that male traits favored by female choice retain substantial amounts of additive genetic variance. We explored this dilemma through an ecological genetic approach and focused on the potential contributions of genotype x environment interaction (GEI) to maintenance of additive genetic variance for male signal characters in the lesser waxmoth, Achroia grisella (Lepidoptera: Pyralidae). We artificially selected genetic variants for two male signal characters, signal rate (SR) and peak amplitude (PA), that influence female attraction and then examined the phenotypic plasticity of these variants (high- and low-SR and high- and low-PA lines) under a range of environmental conditions expected in natural populations. Our split-family breeding experiments indicated that two signal characters, SR and PA, and several developmental characters in both high- and low-SR and high- and low-PA lines displayed considerable phenotypic plasticity among the environments tested. Moreover, strong GEIs leading to crossover between high- and low-SR lines were found for SR and developmental period. Therefore, neither high- nor low-SR genetic variants would achieve maximum attractiveness and fitness in every environment, and those variants producing unattractive signals with low SRs under normal conditions may remain in populations provided that gene flow across environments or generation overlap are sufficiently high. We speculate that the phenotypic plasticity for SR and developmental period is adaptive in A. grisella populations experiencing a range of temperature and density conditions. Females mating with attractive (high-SR) males may be assured of obtaining good genes because these males sire offspring that develop more rapidly and a crossover for developmental period may parallel that for SR. Such parallel crossovers may be expected wherever good-genes sexual selection mechanisms operate.     

An evolutionary limit to male mating success

The well-known phenotypic diversity of male sexual displays, and the high levels of genetic variation reported for individual display traits have generated the expectation that male display traits, and consequently male mating success, are highly evolvable. It has not been shown however that selection for male mating success, exerted by female preferences in an unmanipulated population, results in evolutionary change. Here, we tested the expectation that male mating success is highly evolvable in Drosophila bunnanda using an experimental evolution approach. Female D. bunnanda exhibit a strong, consistent preference for a specific combination of male cuticular hydrocarbons (CHCs). We used female preference to select for male mating success by propagating replicate populations from either attractive or unattractive males over 10 generations. Neither the combination of CHCs under sexual selection (the sexual signal) nor male mating success itself evolved. The lack of a response to selection was consistent with previous quantitative genetic experiments in D. bunnanda that demonstrated the virtual absence of genetic variance in the combination of CHCs under sexual selection. Persistent directional selection, such as applied by female mate choice, may erode genetic variance, resulting in multitrait evolutionary limits.     

Condition-dependence,genotype-by-environment interactions and the lek paradox

The lek paradox states that maintaining genetic variation necessary for 'indirect benefit' models of female choice is difficult, and two interrelated solutions have been proposed. 'Genic capture' assumes condition-dependence of sexual traits, while genotype-by-environment interactions (GEIs) offer an additional way to maintain diversity. However, condition-dependence, particularly with GEIs, implies that environmental variation can blur the relationship between male displays and offspring fitness. These issues have been treated separately in the past. Here we combine them in a population genetic model, and show that predictions change not only in magnitude but also in direction when the timing of dispersal between environments relative to the life cycle is changed. GEIs can dramatically improve the evolution of costly female preferences, but also hamper it if much dispersal occurs between the life history stage where condition is determined and mating. This situation also arises if selection or mutation rates are too high. In general, our results highlight that when evaluating any mechanism promoted as a potential resolution of the lek paradox, it is not sufficient to focus on its effects on genetic variation. It also has to be assessed to what extent the proposed mechanism blurs the association between male attractiveness and offspring fitness; the net balance of these two effects can be positive or negative, and often strongly context-dependent.     

Condition-dependence, genotype-by-environment interactions and the lek paradox

The lek paradox states that maintaining genetic variation necessary for ‘indirect benefit’ models of female choice is difficult, and two interrelated solutions have been proposed. ‘Genic capture’ assumes condition-dependence of sexual traits, while genotype-by-environment interactions (GEIs) offer an additional way to maintain diversity. However, condition-dependence, particularly with GEIs, implies that environmental variation can blur the relationship between male displays and offspring fitness. These issues have been treated separately in the past. Here we combine them in a population genetic model, and show that predictions change not only in magnitude but also in direction when the timing of dispersal between environments relative to the life cycle is changed. GEIs can dramatically improve the evolution of costly female preferences, but also hamper it if much dispersal occurs between the life history stage where condition is determined and mating. This situation also arises if selection or mutation rates are too high. In general, our results highlight that when evaluating any mechanism promoted as a potential resolution of the lek paradox, it is not sufficient to focus on its effects on genetic variation. It also has to be assessed to what extent the proposed mechanism blurs the association between male attractiveness and offspring fitness; the net balance of these two effects can be positive or negative, and often strongly context-dependent.     

Male Courtship Behavior and Weapon Trait as Indicators of Indirect Benefit in the Bean Bug,Riptortus pedestris

Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male–male competition also drives evolution of male traits that represent competitive ability. Because female choice and male–male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male–male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.     

Genotype‐by‐environment interactions underlie the expression of pre‐ and post‐copulatory sexually selected traits in guppies

The role that genotype‐by‐environment interactions (GEIs) play in sexual selection has only recently attracted the attention of evolutionary biologists. Yet GEIs can have profound evolutionary implications by compromising the honesty of sexual signals, maintaining high levels of genetic variance underlying their expression and altering the patterns of genetic covariance among fitness traits. In this study, we test for GEIs in a highly sexually dimorphic freshwater fish, the guppy Poecilia reticulata. We conducted an experimental quantitative genetic study in which male offspring arising from a paternal half‐sibling breeding design were assigned to differing nutritional ‘environments’ (either high or low feed levels). We then determined whether the manipulation of diet quantity influenced levels of additive genetic variance and covariance for several highly variable and condition‐dependent pre‐ and post‐copulatory sexual traits. In accordance with previous work, we found that dietary limitation had strong phenotypic effects on numerous pre‐ and post‐copulatory sexual traits. We also report evidence for significant GEI for several of these traits, which in some cases (area of iridescence and sperm velocity) reflected a change in the rank order of genotypes across different nutritional environments (i.e. ecological crossover). Furthermore, we show that genetic correlations vary significantly between nutritional environments. Notably, a highly significant negative genetic correlation between iridescent coloration and sperm viability in the high food treatment broke down under dietary restriction. Taken together, these findings are likely to have important evolutionary implications for guppies; ecological crossover may influence sexual signal reliability in unstable (nutritional) environments and contribute towards the extreme levels of polymorphism in sexual traits typically reported for this species. Furthermore, the presence of environment‐specific genetic covariance suggests that trade‐offs measured in one environment may not be indicative of genetic constraints in others.     

SEXUAL CONFLICT AND THE MAINTENANCE OF MULTIVARIATE GENETIC VARIATION

Mate choice should erode additive genetic variation in sexual displays, yet these traits often harbor substantial genetic variation. Nevertheless, recent developments in quantitative genetics have suggested that multivariate genetic variation in the combinations of traits under selection may still be depleted. Accordingly, the erosion and maintenance of variation may only be detectable by studying whole suites of traits. One potential process favoring the maintenance of genetic variance in multiple trait combinations is the modification of sexual selection via sexually antagonistic interactions between males and females. Here we consider how interlocus sexual conflict can shape the genetic architecture of male sexual traits in the cricket, Teleogryllus commodus. In this species, the ability of each sex to manipulate insemination success significantly alters the selection acting on male courtship call properties. Using a quantitative genetic breeding design we estimated the additive genetic variation in these traits and then predicted the change in variation due to previously documented patterns of sexual selection. Our results indicate that female choice should indeed deplete multivariate genetic variance, but that sexual conflict over insemination success may oppose this loss of variance. We suggest that changes in the direction of selection due to sexually antagonistic interactions will be an important and potentially widespread factor in maintaining multivariate genetic variation.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia

The spectacular variability that typically characterizes male genital traits has largely been attributed to the role of sexual selection. Among the evolutionary mechanisms proposed to account for this diversity, two processes in particular have generated considerable interest. On the one hand, females may exploit postcopulatory mechanisms of selection to favour males with preferred genital traits (cryptic female choice; CFC), while on the other hand females may evolve structures or behaviours that mitigate the direct costs imposed by male genitalia (sexual conflict; SC). A critical but rarely explored assumption underlying both processes is that male and female reproductive traits coevolve, either via the classic Fisherian model of preference-trait coevolution (CFC) or through sexually antagonistic selection (SC). Here, we provide evidence for this prediction in the guppy (Poecilia reticulata), a polyandrous livebearing fish in which males transfer sperm internally to females via consensual and forced matings. Our results from a paternal half-sibling breeding design reveal substantial levels of additive genetic variation underlying male genital size and morphology—two traits known to predict mating success during non-consensual matings. Our subsequent finding that physically interacting female genital traits exhibit corresponding levels of genetic (co)variation reveals the potential intersexual coevolutionary dynamics of male and female genitalia, thereby fulfilling a fundamental assumption underlying CFC and SC theory.     

Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections

Background

Theoretical studies suggest that direct and indirect selection have the potential to cause substantial evolutionary change in female mate choice. Similarly, sexual selection is considered a strong force in the evolution of male attractiveness and the exaggeration of secondary sexual traits. Few studies have, however, directly tested how female mate choice and male attractiveness respond to selection. Here we report the results of a selection experiment in which we selected directly on female mating preference for attractive males and, independently, on male attractiveness in the guppy, Poecilia reticulata. We measured the direct and correlated responses of female mate choice and male attractiveness to selection and the correlated responses of male ornamental traits, female fecundity and adult male and female survival.

Results

Surprisingly, neither female mate choice nor male attractiveness responded significantly to direct or to indirect selection. Fecundity did differ significantly among lines in a way that suggests a possible sexually-antagonistic cost to male attractiveness.

Conclusions

The opportunity for evolutionary change in female mate choice and male attractiveness may be much smaller than predicted by current theory, and may thus have important consequences for how we understand the evolution of female mate choice and male attractiveness. We discuss a number of factors that may have constrained the response of female choice and male attractiveness to selection, including low heritabilities, low levels of genetic (co)variation in the multivariate direction of selection, sexually-antagonistic constraint on sexual selection and the "environmental covariance hypothesis".

     

The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis

Understanding the evolution of female multiple mating (polyandry) is crucial for understanding sexual selection and sexual conflict. Despite this interest, little is known about its genetic basis or whether genetics influences the evolutionary origin or maintenance of polyandry. Here, we explore the quantitative genetic basis of polyandry in the parasitoid wasp Nasonia vitripennis, a species in which female re-mating has been observed to evolve in the laboratory. We performed a quantitative genetic experiment on a recently collected population of wasps. We found low heritabilities of female polyandry (re-mating frequency after 18 h), low heritability of courtship duration and a slightly higher heritability of copulation duration. However, the coefficients of additive genetic variance for these traits were all reasonably large (CV(A)>7.0). We also found considerable dam effects for all traits after controlling for common environment, suggesting either dominance or maternal effects. Our work adds to the evidence that nonadditive genetic effects may influence the evolution of mating behaviour in Nasonia vitripennis, and the evolution of polyandry more generally.     

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.     

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.     

Variation in the peacock’s train shows a genetic component

Female peafowl (Pavo cristatus) show a strong mating preference for males with elaborate trains. This, however, poses something of a paradox because intense directional selection should erode genetic variation in the males’ trains, so that females will no longer benefit by discriminating among males on the basis of these traits. This situation is known as the ‘lek paradox’, and leads to the theoretical expectation of low heritability in the peacock’s train. We used two independent breeding experiments, involving a total of 42 sires and 86 of their male offspring, to estimate the narrow sense heritabilities of male ornaments and other morphometric traits. Contrary to expectation, we found significant levels of heritability in a trait known to be used by females during mate choice (train length), while no significant heritabilities were evident for other, non-fitness related morphological traits (tarsus length, body weight or spur length). This study adds to the building body of evidence that high levels of additive genetic variance can exist in secondary sexual traits under directional selection, but further emphasizes the main problem of what maintains this variation.     

Female mate choice predicts paternity success in the absence of additive genetic variance for other female paternity bias mechanisms in Drosophila serrata

After choosing a first mate, polyandrous females have access to a range of opportunities to bias paternity, such as repeating matings with the preferred male, facilitating fertilization from the best sperm or differentially investing in offspring according to their sire. Female ability to bias paternity after a first mating has been demonstrated in a few species, but unambiguous evidence remains limited by the access to complex behaviours, sperm storage organs and fertilization processes within females. Even when found at the phenotypic level, the potential evolution of any mechanism allowing females to bias paternity other than mate choice remains little explored. Using a large population of pedigreed females, we developed a simple test to determine whether there is additive genetic variation in female ability to bias paternity after a first, chosen, mating. We applied this method in the highly polyandrous Drosophila serrata, giving females the opportunity to successively mate with two males ad libitum. We found that despite high levels of polyandry (females mated more than once per day), the first mate choice was a significant predictor of male total reproductive success. Importantly, there was no detectable genetic variance in female ability to bias paternity beyond mate choice. Therefore, whether or not females can bias paternity before or after copulation, their role on the evolution of sexual male traits is likely to be limited to their first mate choice in D. serrata.     

Bottleneck Effects on Genetic Variance for Courtship Repertoire

Bottleneck effects on evolutionary potential in mating behavior were addressed through assays of additive genetic variances and resulting phenotypic responses to drift in the courtship repertoires of six two-pair founder-flush lines and two control populations of the housefly. A simulation addressed the complication that an estimate of the genetic variance for a courtship trait (e.g., male performance vigor or the female requirement for copulation) must involve assays against the background behavior of the mating partners. The additive ``environmental' effect of the mating partner's phenotype simply dilutes the net parent-offspring covariance for a trait. However, if there is an interaction with this ``environmental' component, negative parent-offspring covariances can result under conditions of high incompatibility between the population's distributions for male performance and female choice requirements, despite high levels of genetic variance. All six bottlenecked lines exhibited significant differentiation from the controls in at least one measure of the parent-offspring covariance for male performance or female choice (estimated by 50 parent-son and 50 parent-daughter covariances for 10 courtship traits per line) which translated to significant phenotypic drift. However, the average effect across traits or across lines did not yield a significant net increase in genetic variance due to bottlenecks. Concerted phenotypic differentiation due to the founder-flush event provided indirect evidence of directional dominance in a subset of traits. Furthermore, indirect evidence of genotype-environment interactions (potentially producing genotype-genotype effects) was found in the negative parent-offspring covariances predicted by the male-female interaction simulation and by the association of the magnitude of phenotypic drift with the absolute value of the parent-offspring covariance. Hence, nonadditive genetic effects on mating behavior may be important in structuring genetic variance for courtship, although most of the increases in genetic variance would be expected to reflect inbreeding depression with relatively rare situations representing the facilitation of speciation by bottlenecks.     

A Paradox of Genetic Variance in Epigamic Traits: Beyond “Good Genes” View of Sexual Selection

Maintenance of genetic variance in secondary sexual traits, including bizarre ornaments and elaborated courtship displays, is a central problem of sexual selection theory. Despite theoretical arguments predicting that strong sexual selection leads to a depletion of additive genetic variance, traits associated with mating success show relatively high heritability. Here we argue that because of trade-offs associated with the production of costly epigamic traits, sexual selection is likely to lead to an increase, rather than a depletion, of genetic variance in those traits. Such trade-offs can also be expected to contribute to the maintenance of genetic variation in ecologically relevant traits with important implications for evolutionary processes, e.g. adaptation to novel environments or ecological speciation. However, if trade-offs are an important source of genetic variation in sexual traits, the magnitude of genetic variation may have little relevance for the possible genetic benefits of mate choice.     

Good genes and sexual selection in dung beetles (Onthophagus taurus): genetic variance in egg-to-adult and adult viability

Whether species exhibit significant heritable variation in fitness is central for sexual selection. According to good genes models there must be genetic variation in males leading to variation in offspring fitness if females are to obtain genetic benefits from exercising mate preferences, or by mating multiply. However, sexual selection based on genetic benefits is controversial, and there is limited unambiguous support for the notion that choosy or polyandrous females can increase the chances of producing offspring with high viability. Here we examine the levels of additive genetic variance in two fitness components in the dung beetle Onthophagus taurus. We found significant sire effects on egg-to-adult viability and on son, but not daughter, survival to sexual maturity, as well as moderate coefficients of additive variance in these traits. Moreover, we do not find evidence for sexual antagonism influencing genetic variation for fitness. Our results are consistent with good genes sexual selection, and suggest that both pre- and postcopulatory mate choice, and male competition could provide indirect benefits to females.