Testing the prediction from sexual selection of a positive genetic correlation between human mate preferences and corresponding traits

Sexual selection can cause evolution in traits that affect mating success, and it has thus been implicated in the evolution of human physical and behavioural traits that influence attractiveness. We use a large sample of identical and nonidentical female twins to test the prediction from mate choice models that a trait under sexual selection will be positively genetically correlated with preference for that trait. Six of the eight preferences we investigated, i.e. height, hair colour, intelligence, creativity, exciting personality, and religiosity, exhibited significant positive genetic correlations with the corresponding traits, while the personality measures ‘easy going’ and ‘kind and understanding’ exhibited no phenotypic or genetic correlation between preference and trait. The positive results provide important evidence consistent with the involvement of sexual selection in the evolution of these human traits.     

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.     

Mate preferences and choices for facial and body hair in heterosexual women and homosexual men: influence of sex,population, homogamy,and imprinting-like effect

Recent research has reported that male body and facial hair influence women's mate preferences. However, it is not clear whether such preferences are typical for women or for individuals who prefer males as sexual partners. Here we explored body and facial hair in preferred and actual partners among men and women who prefer men as sexual partners. Including homosexual individuals provides a unique opportunity to investigate whether evolved mating psychologies are specific to the sex of the individual or sex of the partner. Based on an online survey of 1577 participants from Brazil and the Czech Republic, we found that, on average, homosexual men preferred hairier stimuli than heterosexual women, supporting past findings that homosexual men have strong preferences for masculine traits. Preferences for facial and body hair appear to be influenced less by sex of the preferred partner than sex of the individual, pointing to a possible sex-specific mating psychology. Further, Brazilians preferred bigger beards than Czechs, which was positively associated with the self-reported amount of beardedness in Brazil, suggesting that familiarity effects underpin cross-cultural differences in preferences for facial hair. Moreover, homosexual men preferred a self-similar degree of beardedness, and Czech women preferred a similar degree of beardedness as their fathers had during their childhood. However, these effects were not associated with the level of facial hair in their actual partners; in general, mate preferences and actual mate choices for facial and body hair differed. Thus, individual differences in some self-reported characteristics, cultural factors, and aspects of personal experience may modulate differences in preferences for masculine traits.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

Experimental evidence that women's mate preferences are directly influenced by cues of pathogen prevalence and resource scarcity

When choosing a mate, women are thought to face a trade-off between genetic and parental quality. Recent research suggests that this trade-off is influenced by environmental factors such as pathogen prevalence and resource scarcity, which affect the relative value of genetic and parental quality to offspring fitness. To further investigate these findings, the current study primed 60 women with pathogen prevalence, resource scarcity or an irrelevant threat, before administering a forced trade-off task that assessed mate preferences for traits thought to be indicative of genetic or parental quality. Women primed with pathogen prevalence revealed greater preferences for traits indicative of genetic quality at the expense of traits indicative of parental quality. The reverse was found for women primed with resource scarcity. These findings suggest that environmental factors may directly influence women's mate preferences owing to evolved plasticity, such that mate preferences are flexible in response to environmental factors.     

The genetic basis of female mate preferences

We review the evidence for genetic variation in female and male mate preferences. Genetic differences between species and partially isolated races show that preferences can evolve and were genetically variable in the past. Within populations there is good evidence of genetic variation, both of discrete genetic effects (8 cases) and quantitative genetic effects (17 cases), from a diverse range of taxa. We also review evidence for the presence of genetic covariance between mate preferences and sexual traits in the other sex. The 11 studies go a long way to validating the theoretical prediction of positive genetic covariance. The few negative results are best explained by a lack of appropriate experimental design. One unresolved question is whether genetic covariance is due to linkage disequilibrium between unlinked genes or physical linkage. Some evidence points to linkage disequilibrium but this is not yet conclusive.     

THE INFLUENCE OF POLLINATOR PHYLOGEOGRAPHY AND MATE PREFERENCE ON FLORAL DIVERGENCE IN A SEXUALLY DECEPTIVE DAISY

Divergent mate preferences and subsequent genetic differentiation between populations has been demonstrated, but its effects on interspecific interactions are unknown. Associated species exploiting these mate preferences, for example, may diverge to match local preferences. We explore this idea in the sexually deceptive, fly‐mimicking daisy, Gorteria diffusa, by testing for association between genetic structure in the fly pollinator (a proxy for mate preference divergence) and geographic divergence in floral form. If genetic structure in flies influences interactions with G. diffusa, we expect phylogeographically distinct flies to be associated with different floral forms. Flies associated with forms exploiting only feeding behavior often belonged to several phylogeographic clades, whereas flies associated with forms exploiting male‐mating behavior always belonged to distinct clades, indicating the possibility of pollinator‐mediated floral divergence through phylogeographic variation in mating preferences of male flies. We tested this hypothesis with reciprocal presentations using male flies from distinct clades associated with separate floral forms. Results show that males from all clades exhibit similar preferences, making pollinator driven divergence through geographic variation in mate preference unlikely. Males, however, showed evidence of learned resistance to deceptive traits, suggesting antagonistic interactions between plants and pollinators may drive deceptive floral trait evolution in G. diffusa.     

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.     

Sexual selection in genetic colour-polymorphic species: a review of experimental studies and perspectives

Sexual selection theory has primarily focussed on the role of mating preferences for the best individuals in the evolution of condition-dependent ornaments, traits that signal absolute quality. Because the most suitable mate for one individual is not always the best for others, however, we argue that non-directional mate choice can promote the evolution of alternative morphs that are not condition-dependent in their expression (i.e. genetic polymorphism). We list the different mate-choice rules (i.e. all individuals have the same preference; preference depends on the chooser’s morph; individuals mate preferentially with conspecifics displaying an uncommon or the most frequent morph) and review experimental studies that investigated mate choice in natural populations of colour-polymorphic animals. Our review emphasises that although the experimental data support the idea that sexual selection plays an important role in the evolution of genetic colour polymorphism in many different ways, little is known about the adaptive value of each mate-choice strategy and about their implication in the evolutionary stability of colour polymorphism. One way of solving this problem is to determine the adaptive function of colour morphs, a worthwhile objective, because better understanding of mate-choice rules in polymorphic species should provide important insights into sexual-selection processes and, in turn, into the maintenance of genetic variation.     

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.     

Similar preferences for ornamentation in opposite‐ and same‐sex choice experiments

Selection due to social interactions comprises competition over matings (sexual selection stricto sensu) plus other forms of social competition and cooperation. Sexual selection explains sex differences in ornamentation and in various other phenotypes, but does not easily explain cases where those phenotypes are similar in males and females. Understanding such similarities requires knowing how phenotypes influence nonsexual social interactions as well, which can be very important in gregarious animals, but whose role for phenotypic evolution has been overlooked. For example, ‘mate choice’ experiments often found preferences for ornamentation, but have not assessed whether those are strictly sexual or are general social preferences. Using choice experiments with a gregarious and mutually ornamented finch, the common waxbill (Estrilda astrild), we show that preferences for ornamentation in the opposite‐sex also extend to same‐sex interactions. Waxbills discriminated between opposite‐ and same‐sex individuals, but most preferences for colour traits were similar when interacting with either sex. Similar preferences in sexual and nonsexual associations may be widespread in nature, either as social adaptations or as by‐product of mate preferences. In either case, such preferences may set the stage for the evolution of mutual ornamentation and of various other similarities between the sexes.     

Correlated changes in male plumage coloration and female mate choice in cardueline finches

The coevolution of extravagant male traits and female mate preferences is a central tenet of sexual selection theory. In lineages in which males have developed more elaborate sexual characters, females favour the most extreme expression of the trait. In some taxa, however, ornamental displays have evolved from more to less exaggerated states. Under these circumstances, it is unclear whether females show preferences for an ancestral male condition or for the current, less elaborate display. Here, we tested female mate preferences relative to male ornamental coloration in two species of cardueline finch (the American goldfinch, Carduelis tristis, and pine siskin, Carduelis pinus) that have evolved less elaborate carotenoid-based colour displays from more elaborately coloured ancestral states. We presented females of each species with a choice of males having either large patches of red colour (the elaborate, ancestral condition) or with species-typical patches of yellow colour (the less elaborate, derived state). Female goldfinches and siskins showed consistent preferences for the natural colour displays of males, and not for the more elaborate, ancestral colour pattern. Previous research on another cardueline finch taxon (a subspecies of the house finch, Carpodacus mexicanus griscomi), however, showed that females prefer more elaborate, ancestral coloration to the current form of reduced colour expression. The lack of congruence between male trait expression and female trait preference in the lineage with the most recently derived reduction in trait expression suggests that there may be evolutionary lags in the correspondence between male traits and female preferences. A shift in the expression of male coloration appears to be the first step towards the evolution of reduced colour displays in these finches.     

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae)

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full‐sibling, split‐family rearing design to estimate genetic correlations (r_G) between fecundity and signal traits, and compared those relationships against population‐level mate preferences for the signal traits. Animal model estimates for r_G between female fecundity and male signal traits overlapped zero—rejecting the hypothesis—but could reflect sample size limitations. The magnitude of r_G correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population‐level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high‐performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.     

The causes of variation in the presence of genetic covariance between sexual traits and preferences

Mating traits and mate preferences often show patterns of tight correspondence across populations and species. These patterns of apparent coevolution may result from a genetic association between traits and preferences (i.e. trait–preference genetic covariance). We review the literature on trait–preference covariance to determine its prevalence and potential biological relevance. Of the 43 studies we identified, a surprising 63% detected covariance. We test multiple hypotheses for factors that may influence the likelihood of detecting this covariance. The main predictor was the presence of genetic variation in mate preferences, which is one of the three main conditions required for the establishment of covariance. In fact, 89% of the nine studies where heritability of preference was high detected covariance. Variables pertaining to the experimental methods and type of traits involved in different studies did not greatly influence the detection of trait–preference covariance. Trait–preference genetic covariance appears to be widespread and therefore represents an important and currently underappreciated factor in the coevolution of traits and preferences.     

Population divergence in chemical signals and the potential for premating isolation between islet- and mainland populations of the Skyros wall lizard (Podarcis gaigeae)

When sexually selected traits diverge because of different local selective environments, premating isolation might arise as a correlated response. However, sexually selected traits might also diverge by stochastic forces. Here, we show that odour-based mate preferences and scent composition have diverged between islet- and mainland populations of Skyros wall lizard, Podarcis gaigeae. We quantified the degree of scent-mediated premating isolation between populations. Islet lizards preferred scent from islet lizards, whereas the mainland populations were less discriminatory. The pheromone compositions differed more between islets than between islet- and mainland populations and did not differ significantly between mainland populations. There was a tendency for population divergence in pheromones to be positively correlated with neutral genetic divergence. This might indicate a role for genetic drift in evolutionary change in these signals and partial decoupling between signals and preferences. Our results suggest that chemical signals and associated mate preferences can diverge through stochastic and selective forces and influence premating isolation.     

Consistency of mate choice in eye and hair colour: Testing possible mechanisms

Partner preferences are formed by several mechanisms, including an imprinting-like effect (parent-similarity) and homogamy (self-similarity). It is still unknown, however, whether these preferences remain stable throughout an individual’s lifetime. We have therefore tested the consistency of mate choice in eye and hair colour both in a shortand long-term context. In other words, we tested whether people systematically choose partners with a particular eye and hair colour. We asked 1,048 respondents to indicate the eye and hair colour of themselves, their opposite-sex and same-sex parent, and all the romantic partners they had in their lives. Our results show that people consistently choose partners of a particular eye and hair colour in both short- and long-term contexts, which suggests that people do have their ‘types’. Nevertheless, the consistency was significantly higher in a long-term context than in a short-term context. Furthermore, the eye colour of one's partner was predicted by the eye colour of one's opposite-sex as well as same-sex parent, but the strongest parental effect was found when both parents had same eye colour. There were no significant results for hair colour. Our results thus suggest that preferences for eye colour are determined by the imprinting-like effect rather than by homogamy, and that they remain stable over time. These findings also indirectly support an assumption of stability of this imprinting-like effect in humans, since people consistently choose partners with their opposite-sex parent's eye-colour.     

Good genes,complementary genes and human mate preferences

The past decade has witnessed a rapidly growing interest in the biological basis of human mate choice. Here we review recent studies that demonstrate preferences for traits which might reveal genetic quality to prospective mates, with potential but still largely unknown influence on offspring fitness. These include studies assessing visual, olfactory and auditory preferences for potential good-gene indicator traits, such as dominance or bilateral symmetry. Individual differences in these robust preferences mainly arise through within and between individual variation in condition and reproductive status. Another set of studies have revealed preferences for traits indicating complementary genes, focussing on discrimination of dissimilarity at genes in the major histocompatibility complex (MHC). As in animal studies, we are only just beginning to understand how preferences for specific traits vary and inter-relate, how consideration of good and compatible genes can lead to substantial variability in individual mate choice decisions and how preferences expressed in one sensory modality may reflect those in another. Humans may be an ideal model species in which to explore these interesting complexities.     

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.     

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner''s heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.     

MATE CHOICE FOR NONADDITIVE GENETIC BENEFITS CORRELATE WITH MHC DISSIMILARITY IN THE ROSE BITTERLING (RHODEUS OCELLATUS)

Good genes models of mate choice predict additive genetic benefits of choice whereas the compatibility hypothesis predicts nonadditive fitness benefits. Here the Chinese rose bitterling, Rhodeus ocellatus, a freshwater fish with a resource‐based mating system, was used to separate additive and nonadditive genetic benefits of female mate choice. A sequential blocked mating design was used to test female mate preferences, and a cross‐classified breeding design coupled with in vitro fertilizations for fitness benefits of mate choice. In addition, the offspring produced by the pairing of preferred and nonpreferred males were reared to maturity and their fitness traits were compared. Finally, the MHC DAB1 gene was typed and male MHC genotypes were correlated with female mate choice. Females showed significant mate preferences but preferences were not congruent among females. There was a significant interaction of male and female genotype on offspring survival, rate of development, growth rate, and body size. No significant male additive effects on offspring fitness were observed. Female mate preferences corresponded with male genetic compatibility, which correlated with MHC dissimilarity. It is proposed that in the rose bitterling genetic compatibility is the mechanism by which females obtain a fitness benefit through mate choice and that male MHC dissimilarity, likely mediated by odor cues, indicates genetic compatibility.