Evolution of a mating preference for a dual‐utility trait used in intrasexual competition in genetically monogamous populations

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.     

Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change

The expression in females of ornaments thought to be the target of sexual selection in males is a long-standing puzzle. Two main hypotheses are proposed to account for the existence of conspicuous ornaments in both sexes (mutual ornamentation): genetic correlation between the sexes and sexual selection on females as well as males. We examined the pattern of ornament gains and losses in 240 species of dragon lizards (Agamidae) in order to elucidate the relative contribution of these two factors in the evolution of mutual ornamentation. In addition, we tested whether the type of shelter used by lizards to avoid predators predicts the evolutionary loss or constraint of ornament expression. We found evidence that the origin of female ornaments is broadly consistent with the predictions of the genetic correlation hypothesis. Ornaments appear congruently in both sexes with some lineages subsequently evolving male biased sexual dimorphism, apparently through the process of natural selection for reduced ornamentation in females. Nevertheless, ornaments have also frequently evolved in both sexes independently. This suggests that genetic correlations are potentially weak for several lineages and sexual selection on females is responsible for at least some evolutionary change in this group. Unexpectedly, we found that the evolutionary loss of some ornaments is concentrated more in males than females and this trend cannot be fully explained by our measures of natural selection.     

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

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

Competition for access to mates predicts female-specific ornamentation and male investment in relative testis size

Sexually selected ornaments are highly variable and the factors that drive variation in ornament expression are not always clear. Rare instances of female-specific ornament evolution (such as in some dance fly species) are particularly puzzling. While some evidence suggests that such rare instances represent straightforward reversals of sexual selection intensity, the distinct nature of trade-offs between ornaments and offspring pose special constraints in females. To examine whether competition for access to mates generally favors heightened ornament expression, we built a phylogeny and conducted a comparative analysis of Empidinae dance fly taxa that display female-specific ornaments. We show that species with more female-biased operational sex ratios in lek-like mating swarms have greater female ornamentation, and in taxa with more ornate females, male relative testis investment is increased. These findings support the hypothesis that ornament diversity in dance flies depends on female receptivity to mates, which is associated with contests for nutritious nuptial gifts provided by males. Moreover, our results suggest that increases in female receptivity lead to higher levels of sperm competition among males. The incidence of both heightened premating sexual selection on females and postmating selection on males contradicts assertions that sex roles are straightforwardly reversed in dance flies.     

The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition

Ornaments, weapons and aggressive behaviours may evolve in female animals by mate choice and intrasexual competition for mating opportunities-the standard forms of sexual selection in males. However, a growing body of evidence suggests that selection tends to operate in different ways in males and females, with female traits more often mediating competition for ecological resources, rather than mate acquisition. Two main solutions have been proposed to accommodate this disparity. One is to expand the concept of sexual selection to include all mechanisms related to fecundity; another is to adopt an alternative conceptual framework-the theory of social selection-in which sexual selection is one component of a more general form of selection resulting from all social interactions. In this study, we summarize the history of the debate about female ornaments and weapons, and discuss potential resolutions. We review the components of fitness driving ornamentation in a wide range of systems, and show that selection often falls outside the limits of traditional sexual selection theory, particularly in females. We conclude that the evolution of these traits in both sexes is best understood within the unifying framework of social selection.     

Male‐Biased Mate Competition in King Penguin Trio Parades

Darwin devised sexual selection theory to explain sexual dimorphisms. Further developments of the theory identified the operational sex‐ratio (OSR) as one of its cornerstones, and it was commonly admitted that an OSR biased toward one sex would lead to stronger selection pressures toward that sex. Recent theoretical developments have challenged this view and showed that the OSR alone does not determine the direction of sexual selection, more particularly in mutually ornamented species exhibiting high and similar parental investment by both sexes. These developments, however, focused on mutual intersexual selection, and little is known about intrasexual selection of both males and females in species exhibiting such characteristics. The first aim of our study was to test the relative involvement of males and females in same‐sex contest over mates in the king penguin, a species exhibiting mutual ornamentation of the sexes, high parental investment by both sexes, and a male‐biased OSR. We investigated the sex composition of trio parades, which are groups of three individuals that compete for mates during pair formation. We found that these trios consist of a female trailed by two fighting males in 19 of 20 cases; the 20th trio was all male. The second aim of our study was to investigate the existence of within‐sex differences in colour ornaments between individuals involved in such trios and individuals already paired. While limited sample sizes precluded detection of statistically significant differences between trios vs. pairs, reflectance measurements suggested that the beak spot of males in trios were more strongly ultraviolet than the beak spot of males in pairs. We concluded that intrasexual selection in our colony follows the typical pattern of mate competition observed in species in which sexual dimorphisms and OSR are male biased, and discussed the ultraviolet difference within the framework of the king penguins' colour perception.     

Evolution of an ornament,the dewlap,in females of the lizard genus Anolis

Male ornaments have been the subject of numerous studies on sexual selection and communication, although female ornaments have garnered substantially less study, even though female ornaments are well developed in some species. The factors that have propelled the evolution of elaborate ornaments in females are poorly understood but may include genetic correlations between the sexes, social selection, sensory drive or species recognition. We used simulation‐based comparative methods and a newly estimated phylogeny to test these four hypotheses to explain female ornamentation within the diverse neotropical lizard genus Anolis. We found support for the sensory drive hypothesis and the social selection hypothesis; the female dewlap was larger in species that use more arboreal habitats, as well as in species where the sexes were less dimorphic. We did not find support for the genetic correlation hypothesis or the species recognition hypothesis. We propose that the size of the female dewlap may evolve in response to sensory drive differentially affecting species in different habitats, as well as social selection such as male mate choice or intrasexual competition for territory among females. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 191–201.     

Patterns of fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

No evidence of assortative mating on the basis of putative ornamental traits in Long‐tailed Finches Poephila acuticauda

When multiple ornaments are expressed in both sexes, they are generally assumed to be maintained by mutual sexual selection and have a function in mate choice. In the Long‐tailed Finch Poephila acuticauda both sexes exhibit multiple ornaments that vary in their expression in either size (pintail and throat patch) or colour (bill) between individuals and sexes. We assessed whether these ornaments are maintained by mutual sexual selection by exploring whether individuals in a wild population paired assortatively with respect to these ornamental traits, and the degree to which the expression of these ornamental traits was indicative of reproductive success. We found no evidence of assortative pairing with respect to variation in homologous ornaments or body condition in the two sexes. In addition, we found no effect of ornament expression on the reproductive success of either males or females. Our findings suggest that the expression of these apparently ornamental traits in both sexes of this species may play no current role in mutual mate selection or as indicator traits of reproductive performance. We are currently unable to identify any function for these very elaborate ornaments in either sex of this species and suggest that the typical assumption that all such traits have an ornamental function may need further examination.     

Mutually honest? Physiological ‘qualities’ signalled by colour ornaments in monomorphic king penguins

Mate choice is expected to be important for the fitness of both sexes for species in which successful reproduction relies strongly on shared and substantial parental investment by males and females. Reciprocal selection may then favour the evolution of morphological signals providing mutual information on the condition/quality of tentative partners. However, because males and females often have differing physiological constraints, it is unclear which proximate physiological pathways guarantee the honesty of male and female signals in similarly ornamented species. We used the monomorphic king penguin (Aptenodytes patagonicus) as a model to investigate the physiological qualities signalled by colour and morphological ornaments known to be under sexual selection (coloration of the beak spots and size of auricular feather patches). In both sexes of this slow‐breeding seabird, we investigated the links between ornaments and multiple indices of individual quality; including body condition, immunity, stress and energy status. In both sexes, individual innate immunity, resting metabolic rate, and the ability to mount a stress response in answer to an acute disturbance (capture) were similarly signalled by various aspects of beak coloration or auricular patch size. However, we also reveal interesting and contrasting relationships between males and females in how ornaments may signal individual quality. Body condition and oxidative stress status were signalled by beak coloration, although in opposite directions for the sexes. Over an exhaustive set of physiological variables, several suggestive patterns indicated the conveyance of honest information about mate quality in this monomorphic species. However, sex‐specific patterns suggested that monomorphic ornaments may signal different information concerning body mass and oxidative balance of males and females, at least in king penguins.     

Dominant females have brighter ornamentation in a sexually dimorphic lekking species

Males often exhibit elaborate ornamentation that contributes to their fitness. Similarly, females can also exhibit elaborate ornamentation, but we have a relatively limited understanding of its function. Recent studies have demonstrated that female ornamentation can function in both intrasexual competition and male mate choice, but few studies have been conducted on lekking species. We therefore investigated the possibility that female ornamentation provides information about the dominance status of the bearer, which could mediate intrasexual competition. We examined this possibility using Indian peafowl (Pavo cristatus), a sexually dimorphic lekking species in which females exhibit elaborate ornamentation in the form of iridescent green neck plumage. We tested whether female ornamentation predicts dominance status using an information theoretic model averaging approach. We found that females with brighter ornamentation are more socially dominant than females with darker ornamentation. These results suggest that female ornamentation in this species provides social information about the dominance status of the bearer. This study provides insight into the evolution of conspicuous female traits by suggesting a potential role for female ornamentation in intrasexual competition in a lekking species.     

Sexually Dimorphic Intrasexual Duetting in an Otherwise Monomorphic Green Lacewing (Neuroptera, Chrysopidae, Chrysoperla plorabunda): Sexual Selection or Sex Recognition?

Songs produced during heterosexual duets in a green lacewing, C. plorabunda, are sexually monomorphic. However, individuals of either sex will also engage in intrasexual duets, which can exhibit sexual dimorphism. We confined males and females together in various combinations in a small arena to study the phenotypes, behavioral interactions, and functional roles of duetting in this species. The goal was to test whether sexual selection or sex recognition provided the better explanation of song sexual dimorphism. We determined that the monomorphic form of the intrasexual duet was long and stable, and could take place either between males or between females. Such “standard” intrasexual duetting songs were acoustically indistinguishable from heterosexual songs. However, males could also engage other males in special “fast duets” that sped up and terminated abruptly. Equivalent fast duets were not part of the female repertory. Fast duetting songs between males differed significantly from other types of male or female duetting songs in every measurable characteristic, but their role in the mating system was ambiguous. Contrary to one prediction of the sexual selection hypothesis, fast duetting between males occurred less often in situations where it might be the most useful to males in securing mates, i.e., during male-male-female interactions (trios). In addition, fast songs that started, ended, both started and ended, or neither started nor ended duets were acoustically indistinguishable, making it unlikely that females were choosing males based on such variation. However, songs that “both started and ended” fast duets were associated with a significant mating advantage, indicating a possible role for fast duetting in male-male sexual competition. Because the alternative hypothesis of sex recognition was also supported by some of our results, we conclude that aggressive qualities of male-male fast duets probably mediate intrasexual selection, while their increasing tempo serves as an adaptive response to promote rapid sex recognition by truncating unproductive and potentially dangerous intrasexual duetting.     

Reproductive skew and female trait elaboration in a cooperatively breeding rail

Intrasexual competition for reproduction is thought to be an important factor in the evolution of ornaments and weapons in males. However, the evolution of morphologically similar traits in females is often explained through other mechanisms, and the role of intrasexual competition in female trait elaboration has received little attention. Here, we explore the factors associated with female trait elaboration in the cooperatively breeding Pukeko (the New Zealand race of the Purple Swamphen Porphyrio porphyrio melanotus) by comparing sexual dimorphism in an ornament across two populations. Importantly, the two populations considered differ in several social factors that could affect the degree of female–female competition, and could thereby produce differential selection on elaborate female traits. Recent studies have suggested that high reproductive skew (i.e. monopolization of reproduction by dominant individuals) could influence the intensity of intrasexual competition and select for female elaboration. However, we found that sexual dimorphism was diminished and Pukeko females had more elaborate ornaments under conditions of low reproductive skew. We discuss alternative factors that could influence the degree of female–female competition, and show that reproductive skew may not always provide an accurate estimate of the scope for intrasexual competition.     

Intrasexual competition in females: evidence for sexual selection?

In spite of recent interest in sexual selection in females, debate exists over whether traits that influence female-female competition are sexually selected. This review uses female-female aggressive behavior as a model behavioral trait for understanding the evolutionary mechanisms promoting intrasexual competition, focusing especially on sexual selection. I employ a broad definition of sexual selection, whereby traits that influence competition for mates are sexually selected, whereas those that directly influence fecundity or offspring survival are naturally selected. Drawing examples from across animal taxa, including humans, I examine 4 predictions about female intrasexual competition based on the abundance of resources, the availability of males, and the direct or indirect benefits those males provide. These patterns reveal a key sex difference in sexual selection: Although females may compete for the number of mates, they appear to compete more so for access to high-quality mates that provide direct and indirect (genetic) benefits. As is the case in males, intrasexual selection in females also includes competition for essential resources required for access to mates. If mate quality affects the magnitude of mating success, then restricting sexual selection to competition for quantity of mates may ignore important components of fitness in females and underestimate the role of sexual selection in shaping female phenotype. In the future, understanding sex differences in sexual selection will require further exploration of the extent of mutual intrasexual competition and the incorporation of quality of mating success into the study of sexual selection in both sexes.     

Mutual mate choice in a female-dominant and sexually monomorphic primate

Sexual dimorphism is common in polygynous species, where intrasexual competition is often thought to drive the evolution of large male body size, and in turn, male behavioral dominance over females. In Madagascar, the entire lemur radiation, which embraces diverse mating systems, lacks sexual dimorphism and exhibits frequent female dominance over males. The evolution of such morphological and behavioral peculiarities, often referred to as "the lemur syndrome," has proven difficult to understand. Among other hypotheses, a potential role of intersexual selection has been repeatedly proposed but hardly ever tested. Here, we investigate whether female choice favors small and compliant males, and whether male choice favors large females in captive gray mouse lemurs (Microcebus murinus). Detailed analysis of a combination of behavioral observations and hormonal data available for both sexes shows that (1) females accept more matings from males with higher fighting abilities, (2) males adjust their investment in intrasexual competition to female fertility, and (3) both male and female strategies are weakly influenced by the body mass of potential partners, in directions contradicting our predictions. These results do not suggest a prominent role of intersexual selection in the evolution and maintenance of the lemur syndrome but rather point to alternative mechanisms relating to male-male competition, specifically highlighting an absence of relationship between male body mass and fighting ability. Finally, our findings add to the growing body of evidence suggesting flexible sex roles, by showing the expression of mutual mate choice in a female-dominant, sexually monomorphic and promiscuous primate.     

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

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

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.     

Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes

Speciation by sexual selection is generally modeled as the coevolution of female preferences and elaborate male ornaments leading to behavioral (sexual) reproductive isolation. One prediction of these models is that female preference for conspecific males should evolve earlier than male preference for conspecific females in sexually dimorphic species with male ornaments. We tested that prediction in darters, a diverse group of freshwater fishes with sexually dimorphic ornamentation. Focusing on the earliest stages of divergence, we tested preference for conspecific mates in males and females of seven closely related species pairs. Contrary to expectation, male preference for conspecific females was significantly greater than female preference for conspecific males. Males in four of the 14 species significantly preferred conspecific females; whereas, females in no species significantly preferred conspecific males. Relationships between the strength of preference for conspecifics and genetic distance revealed no difference in slope between males and females, but a significant difference in intercept, also suggesting that male preference evolves earlier than females’. Our results are consistent with other recent studies in darters and suggest that the coevolution of female preferences and male ornaments may not best explain the earliest stages of behavioral isolation in this lineage.     

Evolution of body colouration in killifishes (Cyprinodontiformes: Aplocheilidae,Nothobranchiidae, Rivulidae): Is male ornamentation constrained by intersexual genetic correlation?

Sexual selection drives the evolution of exaggerated traits in males of many animal species. Nevertheless, the response to this selective pressure can be constrained by genetic correlation between sexes. This hypothesis predicts that costly ornamental structures selected for only in males appear also in females, at least because both sexes share most of their genomes. If a trait bears no fitness advantages to females, its expression should reflect a compromise between selection for hypertrophy in males and natural selection favouring reduction of ornamentation in females. Therefore, extravagant male ornaments should evolve predominantly under weak intersexual genetic correlation. Here, we explore the role and evolutionary stability of the constraint imposed by intersexual genetic correlation in the evolution of body colouration in three species-rich families of killifishes. Across most killifish lineages, the evolutionary changes in male and female variegation were correlated, which identifies intersexual genetic correlation as an important factor in the evolution of killifish colouration. Several lineages overcame the constraining intersexual genetic correlation and evolved extremely conspicuous colouration in males together with plain colouration in females. Hormonal manipulations in two species from closely related genera (Nothobranchius and Fundulopanchax) differing in magnitude of sexual dichromatism suggest that pronounced sexual dimorphism in variegation evolved via disappearance of vivid body colours in females and extension of androgen-linked vivid colouration over body surface in males.     

Precopulatory but not postcopulatory male reproductive traits diverge in response to mating system manipulation in Drosophila melanogaster

Competition between males creates potential for pre‐ and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.