Conflict between direct and indirect benefits of female choice in desert Drosophila

Identifying the factors that contribute to the adaptive significance of mating preferences is one major goal of evolutionary research and is largely unresolved. Both direct and indirect benefits can contribute to mate choice evolution. Failure to consider the interaction between individual consequences of mate choice may obscure the opposing effects of individual costs and benefits. We investigate direct and indirect fitness effects of female choice in a desert fly (Drosophila mojavensis), a species where mating confers resistance to desiccation stress. Females prefer males that provide a direct benefit: greater resistance to desiccation stress. Mating preferences also appear to have indirect consequences: daughters of preferred males have lower reproductive success than daughters of unpreferred males, although additional experimentation will be needed to determine if the indirect consequences of female preferences actually arise from 'sexually antagonistic' variation. Nevertheless, the results are intriguing and are consistent with the hypothesis that an interaction between direct and indirect benefits maintains sexually antagonistic variation in these desert flies: increased desiccation resistance conferred by mating might offset the cost of producing low-fecundity daughters.     

Sexual conflict is not counterbalanced by good genes in the laboratory Drosophila melanogaster model system

Sexual conflict theory is based on the observation that females of many species are harmed through their interactions with males. Direct harm to females, however, can potentially be counterbalanced by indirect genetic benefits, where females make up for a reduction in offspring quantity by an increase in offspring quality through a generic increase in offspring fitness (good genes) and/or one restricted to the context of sexual selection (sexy sons). Here, we quantify the magnitude of the good genes mechanism of indirect benefits in a laboratory-adapted population of Drosophila melanogaster. We find that despite high-standing genetic variance for fitness, females gain at most only a modest benefit through the good genes form of indirect benefits--far too little to counterbalance the direct cost of male-induced harm.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.     

Measuring the fitness benefits of male mate choice in Drosophila melanogaster

It is increasingly realized that the potential for male mate choice is widespread across many taxa. However, measurements of the relative magnitude of the fitness benefits that such choice can confer are lacking. Here, we directly measured, in a comprehensive set of tests that manipulated key variables, the fitness benefits of male mate choice in Drosophila melanogaster by measuring egg production in females that were chosen or rejected by males. The results provided significant evidence for male mate choice. In absolute terms, the observed degree of choice increased male fitness by an average of only 1.59 eggs. However, using a novel technique we show that this benefit of choice represented 14.5% of the maximum potential fitness benefit of choice. The magnitude of mate choice was not significantly altered by variation in (1) mate compatibility, (2) phenotypic plasticity in male mate choice, or (3) whether choosing males were preferred or nonpreferred by females. Overall, we show that male mate choice represents a subtle but significant opportunity for sexual selection, and we offer a novel and widely applicable method for quantifying mate choice.     

Female mate preferences in Drosophila simulans: evolution and costs

Female mate preference is central to sexual selection, and all indirect benefit models require that there is genetic variation in female preference. This has rarely been tested however, with relatively few studies documenting heritable variation in female preference and even fewer that have directly selected on mate preference to unequivocally show that it can evolve. Additionally, costs of mate preference are poorly understood even though these have implications for preference evolution. We selected on female preference for ebony‐males in replicate Drosophila simulans lines, and generated a rapid evolutionary response in both replicates, with the proportion of females mating with ebony‐males increasing from approximately 5% to 30% after five generations of selection. This increase was independent of changes in ebony‐males as only females were included in our selection regime. We could detect no cost to mate preference itself other than that associated with the fitness consequences of mating with ebony males.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.     

Fixed and dilutable benefits: female choice for good genes or fertility

Benefits accruing to females who exercise mate choice have been defined to be either 'direct' or 'indirect'. We suggest an alternative distinction: benefits can be considered 'fixed', meaning they are on average equal to all females mating with the same male (e.g. good genes' benefits) or 'dilutable', meaning they are shared between females mating with the same male, so that the more mates a male has, the lower the average benefit to each (e.g. fertility benefits or many forms of direct benefit). Using a simple model, we show that this distinction has a major effect on the form of female preference. We predict that mating skew will be far greater in species where the benefits are fixed when compared with those where the benefits are dilutable.     

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.     

Meta-analysis suggests choosy females get sexy sons more than "good genes"

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons ("Fisherian" models) or overall fitness of offspring ("good genes" models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta-analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life-history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support "Fisherian" models of preference evolution, while providing equivocal evidence for "good genes." We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.     

The impacts of Wolbachia and the microbiome on mate choice in Drosophila melanogaster

Symbionts and parasites can manipulate their hosts’ reproduction to their own benefit, profoundly influencing patterns of mate choice and evolution of the host population. Wolbachia is one of the most widespread symbionts among arthropods, and one that alters its hosts’ reproduction in diverse and dramatic ways. While we are beginning to appreciate how Wolbachia's extreme manipulations of host reproduction can influence species diversification and reproductive isolation, we understand little about how symbionts and Wolbachia, in particular, may affect intrapopulation processes of mate choice. We hypothesized that the maternally transmitted Wolbachia would increase the attractiveness of its female hosts to further its own spread. We therefore tested the effects of Wolbachia removal and microbiome disruption on female attractiveness and male mate choice among ten isofemale lines of Drosophila melanogaster. We found variable effects of general microbiome disruption on female attractiveness, with indications that bacteria interact with hosts in a line‐specific manner to affect female attractiveness. However, we found no evidence that Wolbachia influence female attractiveness or male mate choice among these lines. Although the endosymbiont Wolbachia can greatly alter the reproduction of their hosts in many species, there is no indication that they alter mate choice behaviours in D. melanogaster.     

Heritability of preferences for multiple cues of mate quality in humans

Human mate preferences have received a great deal of attention in recent decades because of their centrality to sexual selection, which is thought to play a substantial role in human evolution. Most of this attention has been on universal aspects of mate preferences, but variation between individuals is less understood. In particular, the relative contribution of genetic and environmental influences to variation in mate preferences is key to sexual selection models but has barely been investigated in humans, and results have been mixed in other species. Here, we used data from over 4000 mostly female twins who ranked the importance of 13 key traits in a potential partner. We used the classical twin design to partition variation in these preferences into that due to genes, family environment, and residual factors. In women, there was significant variability in the broad-sense heritability of individual trait preferences, with physical attractiveness the most heritable (29%) and housekeeping ability the least (5%). Over all the trait preferences combined, broad-sense heritabilities were highly significant in women and marginally significant in men, accounting for 20% and 19% of the variation, respectively; family environmental influences were much smaller. Heritability was a little higher in reproductive aged than in nonreproductive aged women, but the difference was not significant.     

Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them

“Good genes” models of mate choice are commonly tested by examining whether attractive males sire offspring with improved survival. If offspring do not survive better (or indeed survive less well), but instead inherit the attractiveness of their father, results are typically interpreted to support the Fisherian process, which allows the evolution of preferences for arbitrary traits. Here, I show that the above view is mistaken. Because of life‐history trade‐offs, an attractive male may perform less well in other components of fitness. A female obtains a “good genes” benefit whenever males show heritable variation in quality, even if high‐quality males invest so much in sexual advertisement that attractiveness has no positive correlation with any other life‐history trait than male mating success itself. Therefore, a negative correlation between attractiveness and viability does not falsify good genes, if mating with a high‐quality male results on average in superior offspring performance (mating success of sons included). The heritable “good genes” benefit can be sustained even if sexually antagonistic genes cause female offspring sired by high‐quality males to survive and reproduce less well. Neglecting the component of male mating success from measurements of fitness returns from sons and daughters will bias the advantage of mating with a high‐quality male downwards. This result may partly account for the rather weak “good genes” effects found in a recent meta‐analysis.     

No direct or indirect benefits to cryptic female choice in house crickets (Acheta domesticus)

Cryptic female choice in crickets occurs through the prematureremoval of a male's spermatophore after copulation, which terminatessperm transfer. Although it is known that this behavior candirectly influence the paternity of offspring, its effects onfemale fitness have not been directly assessed. We tested thehypothesis that spermatophore removal by female house crickets(Acheta domesticus) confers fitness benefits on females, byrandomly assigning mates to females but permitting some femalesto freely remove spermatophores after mating (cryptic-choicetreatment) while forcing others to accept complete ejaculates(no-choice treatment). Although there was about a two-fold differencein the volume of ejaculate received by females of the two treatments,there were no significant differences in female longevity, reproductiveoutput, or offspring quality, as measured by offspring massand developmental time. Although differential spermatophoreremoval by females imposes strong sexual selection on males,the absence of a clear treatment effect suggests that femalesobtain no direct or indirect genetic benefits through theirpostcopulatory mating preferences.     

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.     

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

Major histocompatibility complex (MHC)‐associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC‐associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC‐dependent mate choice occurs across the order in a variety of socio‐sexual systems and favours mates with dissimilar, diverse or specific genotypes non‐exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.     

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by-product of sexual conflict over the mating rate.     

Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus)

Abstract Females may choose more attractive mates to obtain better viability or attractiveness genes for their offspring. A number of studies have demonstrated a positive relationship between paternal attractiveness and offspring quality. However, this pattern could be due to inheritance of paternal genes and/or it could be due to increased maternal investment in the offspring of more attractive males. To isolate female responses to male appearance from paternal genetic effects, I housed female red junglefowl ( Gallus gallus ) with vasectomized (sterile) males and artificially inseminated them. Male junglefowl with larger combs are more attractive to females. Females laid more eggs when housed with a large-combed, as opposed to a small-combed, vasectomized mate. Neither egg volume nor offspring body condition was associated with comb size of the mother's vasectomized mate. Paternal genetics appeared important. Body condition and comb size were greater for the sons of large-combed sperm donor males. This is consistent with the hypothesis that genetic benefits to offspring maintain female preference for the most ornate males. It is possible that greater body condition and comb size in sons of large-combed sires was not caused by genetic differences, but instead was due to compounds in the ejaculate of large-combed sperm donors inducing greater reproductive investment from females. However, females artificially inseminated by large-combed males did not produce more or larger eggs than females artificially inseminated by small-combed males, and thus there is no other evidence consistent with ejaculate-induced differential investment. Furthermore, only in older chicks was body condition significantly related to sire comb size, suggesting genetic rather than differential investment mechanisms.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.