Nongenetic inheritance and the evolution of costly female preference

In species where males provide neither direct benefits nor paternal care, it is typically assumed that female preferences are maintained by indirect selection reflecting genetic benefits to offspring of preferred males. However, it remains unclear whether populations harbour sufficient genetic variation in fitness to support costly female preferences – a problem called the ‘lek paradox’. Here, we ask whether indirect selection on female preferences can be maintained by nongenetic inheritance. We construct a general model that can be used to represent either genetic or nongenetic inheritance, depending on the choice of parameter values. Interestingly, we find that costly preference is most likely to evolve and persist when fitness depends on an environmentally induced factor that can be transmitted over a single generation only, such as an environment‐dependent paternal effect. Costly preference can also be supported when fitness depends on a highly mutable factor that can persist over multiple generations, such as an epigenetic mark, but the necessary conditions are more restrictive. Our findings show that nongenetic inheritance provides a plausible hypothesis for the maintenance of costly female preferences in species where males provide no direct benefits to females. Nongenetic paternal inheritance of fitness can occur in species lacking conventional forms of paternal care. Indeed, transmission of paternal condition via sperm‐borne nongenetic factors may be more likely to evolve than conventional forms of paternal investment because sperm‐borne effects are protected from cuckoldry. Our results furnish a novel example of an interaction between genetic and nongenetic inheritance that can lead to otherwise unexpected evolutionary outcomes.     

Mate choice for nonadditive genetic benefits and the maintenance of genetic diversity in song sparrows

The lek paradox asserts that strong directional selection via female choice should deplete additive genetic variation in fitness and consequently any benefit to females expressing the preference. Recently, we have provided a novel resolution to the paradox by showing that nonadditive genetic effects such as overdominance can be inherited from parent to offspring, and populations with females that express a mating preference for outbred males maintain higher genetic variation than populations with females that mate randomly. Here, we test our dynamic model using empirical data previously published from a small island population of song sparrows (Melospiza melodia). The model assumes that fitness and male trait expression display overdominance effects. The results demonstrate that female choice for outbred males mediated by directional selection on song repertoire size provides a heritable benefit to offspring through reduced inbreeding depression. Within the population, we estimate the heritability of the inbreeding coefficient to be 0.18 ± 0.08 (SD). Furthermore, we show that mate choice for outbred males increases fitness‐related genetic variation in the population by 12% and thereby reduces inbreeding depression by 1% per generation in typical years and upwards of 15% in severe years. Thus, mate choice may help to stave off population extinction in this and other small populations.     

EVOLUTION OF MATE CHOICE FOR GENOME-WIDE HETEROZYGOSITY

The extent to which indirect genetic benefits can drive the evolution of directional mating preferences for more ornamented mates, and the mechanisms that maintain such preferences without depleting genetic variance, remain key questions in evolutionary ecology. We used an individual-based genetic model to examine whether a directional preference for mates with higher genome-wide heterozygosity ( H ), and consequently greater ornamentation, could evolve and be maintained in the absence of direct fitness benefits of mate choice. We specifically considered finite populations of varying size and spatial genetic structure, in which parent–offspring resemblance in heterozygosity could provide an indirect benefit of mate choice. A directional preference for heterozygous mates evolved under broad conditions, even given a substantial direct cost of mate choice, low mutation rate, and stochastic variation in the link between individual heterozygosity and ornamentation. Furthermore, genetic variance was retained under directional sexual selection. Preference evolution was strongest in smaller populations, but weaker in populations with greater internal genetic structure in which restricted dispersal increased local inbreeding among offspring of neighboring females that all preferentially mated with the same male. These results suggest that directional preferences for heterozygous or outbred mates could evolve and be maintained in finite populations in the absence of direct fitness benefits, suggesting a novel resolution to the lek paradox.     

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?     

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.     

A potential resolution to the lek paradox through indirect genetic effects

Females often prefer males with elaborate traits, even when they receive no direct benefits from their choice. In such situations, mate discrimination presumably has genetic advantages; selective females will produce offspring of higher genetic quality. Over time, persistent female preferences for elaborate secondary-sexual traits in males should erode genetic variance in these traits, eventually eliminating any benefit to the preferences. Yet, strong female preferences persist in many taxa. This puzzle is called the lek paradox and raises two primary questions: do females obtain genetic benefits for offspring by selecting males with elaborate secondary-sexual characteristics and, if so, how is the genetic variation in these male traits maintained? We suggest that indirect genetic effects may help to resolve the lek paradox. Maternal phenotypes, such as habitat selection behaviours and offspring provisioning, often influence the condition and the expression of secondary-sexual traits in sons. These maternal influences are commonly genetic based (i.e. they are indirect genetic effects). Females choosing mates with elaborate traits may receive ‘good genes’ for daughters in the form of effective maternal characteristics. Recognizing the significance of indirect genetic effects may be important to our understanding of the process and consequences of sexual selection.     

The costs of choice in sexual selection

In Fisher's model of sexual selection female mating preferences are not subject to direct selection but evolve purely because they are genetically correlated with the favoured male trait. But when female choice is costly relative to random mating, for example in energy, time or predation risks, the evolution of female mating preference is subject also to direct selection. With costly female choice the set or line of equilibria found in models of Fisher's process no longer exists. On the line the male trait is under zero net selection, and there is no advantage for a female choosing a male with a more exaggerated character. Therefore any cost to choice causes choosiness to decline. In turn this lowers the strength of sexual selection and the male trait declines as well. So when Fisher's process is the sole force of sexual selection and female choice is costly, only transitory increases in female choice and the preferred male trait are possible. It has often been claimed that exaggerated male characters act as markers or revealers of the genetic quality of potential mates. If females choose their mates using traits that correlate with heritable viability differences then stable exaggeration of both female choice and the preferred male character is possible, even when female choice is costly. The offspring of choosy females have not only a Fisherian reproductive advantage but also greater viability. This suggests that in species with exaggerated male ornamentation, in which female choice is costly, it is likely that female mate choice will be for traits that correlate with male genetic quality.     

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.     

Positive genetic correlation between female preference and offspring fitness

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.     

The heritability of fitness: Bad news for 'good genes'?

Some models of sexual selection depend on a female preference for 'good genes': females choose conspicuous males as these are advertising their possession of genes for fitness characters which can be inherited by their offspring. In contrast, Fisher's fundamental theorem of natural selection - which underlies much of population genetics theory - predicts that in a population at equilibrium there can be no additive genetic variation in fitness. Recent work on collared flycatchers in the wild shows that characters influencing fitness do indeed have a relatively low heritability. However, other studies of the inheritance of fitness in the laboratory suggest that under some circumstances a population may retain considerable genetic diversity for fitness characters. Genetically based female choice might hence have the potential to control the evolution of male sexual ornaments. More work on natural populations is needed; and birds may be a good place to start looking.     

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.     

Queuing in space and time reduces the lek paradox on an antelope lek

Lek systems, where females often use centrality to assess male quality, highlight a general paradox in evolutionary biology: how can female preferences for males providing good genes persist when consequential strong directional selection is predicted to deplete additive genetic variance in male quality and thereby obliterate benefits of choosiness? An explanation contributing to the resolution of this lek paradox may be that genetic variance is retained when an indirect mate choice cue, such as centrality on a lek, is an imperfect indicator of male genetic quality. Here I investigate whether the presence of alternative male mating tactics limits the reliability of centrality as a quality indicator in lek-breeding topi antelopes. Whereas males establishing territories directly on the central lek were relatively large, smaller peripheral males regularly shifted their territories centripetally and in this way also occasionally obtained central territories. By such opportunistic queuing, small males could increase their mating success drastically; however, their territorial tenure in the lek centre was relatively short, consistent with moderate competitive ability. These results suggest that male topi antelopes can obtain central lek territories through alternative mating tactics, providing scope for variance in male quality on the central lek. In a separate finding, the mating success of central males was found to increase during territorial tenure, independent of estimated age. The demonstration of queuing in both space and time on a mammalian lek highlights the importance of considering male tactical dynamics over time in order to avoid an inflated appearance of the lek paradox.     

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.     

The capture of heritable variation for genetic quality through social competition

In theory, females of many species choose mates based on traits that are indicators of male genetic quality. A fundamental question in evolutionary biology is why genetic variation for such indicator traits persists despite strong persistent selection imposed by female preference, which is known as the lek paradox. One potential solution to the lek paradox suggests that the traits that are targets of mate choice should evolve condition-dependent expression and that condition should have a large genetic variance. Condition is expected to exhibit high genetic variance because it is affected by a large number of physiological processes and hence, condition-dependent traits should 'capture' variation contributed by a large number of loci. We suggest that a potentially important cause of variation in condition is competition for limited resources. Here, we discuss a pair of models to analyze the evolutionary genetics of traits affected by success in social competition for resources. We show that competition can contribute to genetic variation of 'competition-dependent' traits that have fundamentally different evolutionary properties than other sources of variation. Competition dependence can make traits honest indicators of genetic quality by revealing the relative competitive ability of males, can provide a component of heritable variation that does not contribute to trait evolution, and can help maintain heritable variation under directional selection. Here we provide a general introduction to the concept of competition dependence and briefly introduce two models to demonstrate the potential evolutionary consequences of competition-dependent trait expression.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

Male killing can select for male mate choice: a novel solution to the paradox of the lek

In lekking species, intense directional selection is applied to aspects of the male genotype by female choice. Under conventional quantitative genetics theory, the expectation is that this will lead to a rapid loss in additive genetic variance for the trait in question. However, despite female choice, male variation is maintained and hence it pays females to continue choosing. This has been termed the ''paradox of the lek''. Here we present a theoretical analysis of a putative sex-role-reversed lek in the butterfly Acraea encedon. Sex-role reversal appears to have come about because of infection with a male-killing Wolbachia. The bacterium is highly prevalent in some populations, such that there is a dearth of males. Receptive females form dense aggregations, and it has been suggested that males preferentially select females uninfected with the bacterium. As with more conventional systems, this presents a theoretical problem exactly analogous to the lek paradox, namely what maintains female variation and hence why do males continue to choose? We model the evolution of a male choice gene that allows discrimination between infected and uninfected females, and show that the stable maintenance of both female variation and male choice is likely, so long as males make mistakes when discriminating between females. Furthermore, our model allows the maintenance, in a panmictic population, of a male killer that is perfectly transmitted. This is the first model to allow this result, and may explain the long-term persistence of a male killer in Hypolimnas bolina.     

Why do ovigerous females approach courting males? Female preferences and sensory biases in a fiddler crab

Perceptual biases explain the origin and evolution of female preference in many species. Some responses that mediate mate choice, however, may have never been used in nonmating contexts. In the fiddler crab, Uca mjoebergi, mate‐searching females prefer faster wave rates and leading wave; however, it remains unclear whether such responses evolved in a mating context (i.e., the preference has effect on the fitness of the female and her offspring that arise from mating with a particular male) or a nonmating contexts (i.e., a female obtains direct benefits through selecting the male with a more detectable trait). Here, we compared the preferences of mate‐searching with those of ovigerous females that are searching for a burrow and do not concern about male “quality.” Results showed that as both mate‐searching and ovigerous females preferentially approached robotic males with faster wave rates. This suggests that wave rate increases detectability/locatability of males, but the mating preference for this trait is unlikely to evolve in the mating context (although it may currently function in mate choice), as it does not provide fitness‐related benefit to females or her offspring. Wave leadership, in contract, was attractive to mate‐searching females, but not ovigerous females, suggesting that female preference for leadership evolves because wave leadership conveys information about male quality. We provide not only an empirical evidence of sensory biases (in terms of the preference for faster wave), but the first experimental evidence that mating context can be the only selection force that mediates the evolution of male sexual traits and female preference (in terms of the preference for leading wave).     

Genetic quality and sexual selection: an integrated framework for good genes and compatible genes

Why are females so choosy when it comes to mating? This question has puzzled and marveled evolutionary and behavioral ecologists for decades. In mating systems in which males provide direct benefits to the female or her offspring, such as food or shelter, the answer seems straightforward — females should prefer to mate with males that are able to provide more resources. The answer is less clear in other mating systems in which males provide no resources (other than sperm) to females. Theoretical models that account for the evolution of mate choice in such nonresource-based mating systems require that females obtain a genetic benefit through increased offspring fitness from their choice. Empirical studies of nonresource-based mating systems that are characterized by strong female choice for males with elaborate sexual traits (like the large tail of peacocks) suggest that additive genetic benefits can explain only a small percentage of the variation in fitness. Other research on genetic benefits has examined nonadditive effects as another source of genetic variation in fitness and a potential benefit to female mate choice. In this paper, we review the sexual selection literature on genetic quality to address five objectives. First, we attempt to provide an integrated framework for discussing genetic quality. We propose that the term ‘good gene’ be used exclusively to refer to additive genetic variation in fitness, ‘compatible gene’ be used to refer to nonadditive genetic variation in fitness, and ‘genetic quality’ be defined as the sum of the two effects. Second, we review empirical approaches used to calculate the effect size of genetic quality and discuss these approaches in the context of measuring benefits from good genes, compatible genes and both types of genes. Third, we discuss biological mechanisms for acquiring and promoting offspring genetic quality and categorize these into three stages during breeding: (i) precopulatory (mate choice); (ii) postcopulatory, prefertilization (sperm utilization); and (iii) postcopulatory, postfertilization (differential investment). Fourth, we present a verbal model of the effect of good genes sexual selection and compatible genes sexual selection on population genetic variation in fitness, and discuss the potential trade-offs that might exist between mate choice for good genes and mate choice for compatible genes. Fifth, we discuss some future directions for research on genetic quality and sexual selection.     

Mate choice for non-additive genetic benefits: a resolution to the lek paradox

In promiscuous mating systems, females often show a consistent preference to mate with one or a few males, presumably to acquire heritable genetic benefits for their offspring. However, strong directional selection should deplete additive genetic variation in fitness and consequently any benefit to expressing the preference by females (referred to as the lek paradox). Here, we provide a novel resolution that examines non-additive genetic benefits, such as overdominance or inbreeding, as a source of genetic variation. Focusing on the inbreeding coefficient f and overdominance effects, we use dynamic models to show that (1) f can be inherited from sire to offspring, (2) populations with females that express a mating preferences for outbred males (low f) maintain higher genetic variation than populations with females that mate randomly, and (3) preference alleles for outbred males can invade populations even when the alleles are associated with a fecundity cost. We show that non-additive genetic variation due to overdominance can be converted to additive genetic variation and becomes “heritable” when the frequencies of alternative homozygous genotypes at fitness loci deviate from equality. Unlike previous models that assume an infinite population size, we now show that genetic drift in finite populations can lead to the necessary deviations in the frequencies of homozygous genotypes. We also show that the “heritability of f,” and hence the benefit to a mating preference for non-additive genetic benefits, is highest in small populations and populations in which a smaller number of loci contribute to fitness via overdominance. Our model contributes to the solution of the lek paradox.