Sexual selection and its evolutionary consequences in female animals

For sexual selection to act on a given sex, there must exist variation in the reproductive success of that sex as a result of differential access to mates or fertilisations. The mechanisms and consequences of sexual selection acting on male animals are well documented, but research on sexual selection acting on females has only recently received attention. Controversy still exists over whether sexual selection acts on females in the traditional sense, and over whether to modify the existing definition of sexual selection (to include resource competition) or to invoke alternative mechanisms (usually social selection) to explain selection acting on females in connection with reproduction. However, substantial evidence exists of females bearing characters or exhibiting behaviours that result in differential reproductive success that are analogous to those attributed to sexual selection in males. Here we summarise the literature and provide substantial evidence of female intrasexual competition for access to mates, female intersexual signalling to potential mates, and postcopulatory mechanisms such as competition between eggs for access to sperm and cryptic male allocation. Our review makes clear that sexual selection acts on females and males in similar ways but sometimes to differing extents: the ceiling for the elaboration of costly traits may be lower in females than in males. We predict that current and future research on female sexual selection will provide increasing support for the parsimony and utility of the existing definition of sexual selection.     

Perspective: female remating,operational sex ratio,and the arena of sexual selection in Drosophila species

Abstract.— As commonly observed among closely related species within a variety of taxa, Drosophila species differ considerably in whether they exhibit sexual dimorphism in coloration or morphology. Those Drosophila species in which male external sexual characters are minimal or absent tend, instead, to have exaggerated ejaculate traits such as sperm gigantism or seminal nutrient donations. Underlying explanations for the interspecific differences in the presence of external morphological sexual dimorphism versus exaggerated ejaculate traits are addressed here by examining the opportunity for sexual selection on males to occur before versus after mating in 21 species of Drosophila . Female remating frequency, an important component of the operational sex ratio, differs widely among Drosophila species and appears to dictate whether the arena of sexual selection is prior to, as opposed to after, copulation. Infrequent female mating results in fewer mating opportunities for males and thus stronger competition for receptive females that favors the evolution of male characters that maximize mating success. On the other hand, rapid female remating results in overlapping ejaculates in the female reproductive tract, such that ejaculate traits which enhance fertilization success are favored. The strong association between female remating frequency in a given species and the presence of sexually selected external versus internal male characters indicates that the relationship be examined in other taxa as well.     

Temporal variation in selection on male and female traits in wild tree crickets

Understanding temporal variation in selection in natural populations is necessary to accurately estimate rates of divergence and macroevolutionary processes. Temporal variation in the strength and direction of selection on sex‐specific traits can also explain stasis in male and female phenotype and sexual dimorphism. I investigated changes in strength and form of viability selection (via predation by wasps) in a natural population of male and female tree crickets over 4 years. I found that although the source of viability stayed the same, viability selection affected males and females differently, and the strength, direction and form of selection varied considerably from year to year. In general, males experienced significant linear selection and significant selection differentials more frequently than females, and different male traits experienced significant linear selection each year. This yearly variation resulted in overall weak but significant convex selection on a composite male trait that mostly represented leg size and wing width. Significant selection on female phenotype was uncommon, but when it was detected, it was invariably nonlinear. Significant concave selection on traits representing female body size was observed in some years, as the largest and smallest females were preyed on less (the largest may have been too heavy for flying wasps to carry). Viability selection was significantly different between males and females in 2 of 4 years. Although viability selection via predation has the potential to drive phenotypic change and sexual dimorphism, temporal variation in selection may maintain stasis.     

Contrasting sexual selection on males and females in a role-reversed swarming dance fly, Rhamphomyia longicauda Loew (Diptera: Empididae)

Although there are several hypotheses for sex-specific ornamentation, few studies have measured selection in both sexes. We compare sexual selection in male and female dance flies, Rhamphomyia longicauda (Diptera: Empididae). Swarming females display size-enhancing abdominal sacs, enlarged wings and decorated tibiae, and compete for nuptial gifts provided by males. Males preferentially approach large females, but the nature of selection and whether it is sex-specific are unknown. We found contrasting sexual selection for mating success on structures shared by males and females. In females, long wings and short tibiae were favoured, whereas males with short wings and long tibiae had a mating advantage. There was no assortative mating. Females occupying potentially advantageous swarm positions were large and, in contrast to selection for mating success, tended to have larger tibiae than those of rivals. We discuss our findings in the context of both the mating biology of dance flies, and the evolution of sexual dimorphism in general.     

Spatiotemporal variation in selection on body size in the dung fly Sepsis cynipsea

Standardized measures of the strength of selection on a character allow quantitative comparisons across populations in time and space. Spatiotemporal variation in selection influences patterns of adaptation and the evolution of characters and must therefore be documented. For the dung-breeding fly Sepsis cynipsea, we document patterns of variation in sexual, fecundity and larval and adult viability selection on body size at several spatiotemporal scales: between-populations, over the season, over the day and between dung pats. Adult viability selection based on residual physiological survivorship in the laboratory was nil or weakly negative. In contrast, larval viability selection in two laboratory environments was weakly positive for males at low competition and females at high competition. Fecundity selection was positive and strong at all times and in all populations. Sexual selection reflecting pairing success was overall strongly positive (about three times stronger than fecundity selection), while selection reflecting male reproductive success via the clutch size of his mate (i.e. assortative mating) was essentially nil. Only sexual selection varied significantly at coarse (between populations and seasonally) but not at fine (within a day or between pats on a pasture) spatial and temporal scales. Quadratic and correlational selection differentials were low and inconsistent in all episodes except for fecundity selection, where there was some evidence that clutch size reaches an asymptote at large body sizes, implying weaker selection for large size as females get bigger. Implications of these results for the evolution of body size and body size dimorphism are discussed.     

CORRELATED EVOLUTION OF MIGRATION AND SEXUAL DICHROMATISM IN THE NEW WORLD ORIOLES (ICTERUS)

The evolution of sexual dimorphism has long been attributed to sexual selection, specifically as it would drive repeated gains of elaborate male traits. In contrast to this pattern, New World oriole species all exhibit elaborate male plumage, and the repeated gains of sexual dichromatism observed in the genus are due to losses of female elaboration. Interestingly, most sexually dichromatic orioles belong to migratory or temperate‐breeding clades. Using character scoring and ancestral state reconstructions from two recent studies in Icterus, we tested a hypothesis of correlated evolution between migration and sexual dichromatism. We employed two discrete phylogenetic comparative approaches: the concentrated changes test and Pagel's discrete likelihood test. Our results show that the evolution of these traits is significantly correlated (CCT: uncorrected P < 0.05; ML: LRT = 12.470, P < 0.005). Indeed, our best model of character evolution suggests that gains of sexual dichromatism are 23 times more likely to occur in migratory taxa. This study demonstrates that a life‐history trait with no direct relationship with sexual selection has a strong influence on the evolution of sexual dichromatism. We recommend that researchers further investigate the role of selection on elaborate female traits in the evolution of sexual dimorphism.     

Stabilizing sexual selection for female ornaments in a dance fly

Ornamental traits function by improving attractiveness and are generally presumed to experience directional selection for mating success. However, given the greater investment of females in offspring than males, female-specific ornaments can in theory signal fecundity yet be constrained by fecundity costs. Theoretical work predicts that such constraints can lead to stabilizing selection via male choice for intermediately ornamented females. Female dance flies Rhamphomyia longicauda (Diptera: Empididae) display two female-specific ornaments in mating swarms - inflatable abdominal sacs and pinnate tibial scales. We investigated the intensity and form of sexual selection on female traits including ornaments and found no evidence for directional sexual selection. Instead, we found marginally nonsignificant quadratic selection for all three measures of ornament expression. Canonical analysis confirmed that the strongest vectors of nonlinear selection were associated with ornamental traits, although the significance of the quadratic coefficients associated with these vectors depended on the statistical approach. Direct Mitchell-Olds and Shaw tests for the location of the maximum fitted fitness value for both raw morphological traits and canonical axes revealed only one marginally nonsignificant result for the multivariate axis loading most heavily on pinnate leg scales. Together, these results provide the first tentative support for stabilizing selection on female-specific ornaments.     

Sexual selection constrains the body mass of male but not female mice

Sexual size dimorphism results when female and male body size is influenced differently by natural and sexual selection. Typically, in polygynous species larger male body size is thought to be favored in competition for mates and constraints on maximal body size are due to countervailing natural selection on either sex; however, it has been postulated that sexual selection itself may result in stabilizing selection at an optimal mass. Here we test this hypothesis by retrospectively assessing the influence of body mass, one metric of body size, on the fitness of 113 wild‐derived house mice (Mus musculus) residing within ten replicate semi‐natural enclosures from previous studies conducted by our laboratory. Enclosures possess similar levels of sexual selection, but relaxed natural selection, relative to natural systems. Heavier females produced more offspring, while males of intermediate mass had the highest fitness. Female results suggest that some aspect of natural selection, absent from enclosures, acts to decrease their body mass, while the upper and lower boundaries of male mass are constrained by sexual selection.     

Ontogenetic variation in the plumage colour of female European Pied Flycatchers Ficedula hypoleuca

Although variation in the dorsal plumage colour of male European Pied Flycatchers Ficedula hypoleuca has received a great deal of attention, females of the species have been usually considered to be nearly uniformly monochromatic brown. Using reflectance spectrophotometry, we explore the age‐dependent variation of plumage colour in females. We disentangle the within‐ and between‐individual effects of this pattern and show a within‐individual darkening of the mantle colour with age, whereas differences between individuals in structural colour expression may underlie the trend for a more reflective white in the females' breast plumage with advancing age. The darkening of the dorsal plumage as females age reflects the most common pattern of age‐related variation in males in most European populations of the species.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Darwinian balancing selection: Predation counters sexual selection in a wild insect

The potential viability costs of sexually selected traits are central to hypotheses about the evolution of exaggerated traits. Estimates of these costs in nature can come from selection analyses using multiple components of fitness during the same time frame. For a population of tree crickets (Oecanthus nigricornis: Gryllidae), we analyzed viability and sexual selection on male traits by comparing Oecanthus prey of a solitary wasp to those that survived, and comparing mating individuals to solitary males. We measured forewing width (sexually size dimorphic and used for singing), head width, pronotum length, and size of hind jumping legs as potential targets of selection. Supporting the hypothesis that sexually selected traits have viability costs, we found that significant directional sexual selection for wider heads was opposed by significant viability selection for narrower heads. Nonlinear selection revealed that individuals with wide heads and small legs were most attractive, but individuals with narrow heads, large legs, and intermediate pronotum length were most likely to survive. Successful mating may put males at greater risk of predation, especially if copulation per se is risky. Such balancing selection in tree crickets may have constrained the evolution of sexual dimorphism in head size—a condition seen in other gryllids and orthopterans.     

Female-specific resource limitation does not make the opportunity for selection more female biased

Competition for limiting resources and stress can magnify variance in fitness and therefore selection. But even in a common environment, the strength of selection can differ across the sexes, as their fitness is often limited by different factors. Indeed, most taxa show stronger selection in males, a bias often ascribed to intense competition for access to mating partners. This sex bias could reverberate on many aspects of evolution, from speed of adaptation to genome evolution. It is unclear, however, whether stronger opportunity for selection in males is a pattern robust to sex-specific stress or resource limitation. We test this in the model species Callosobruchus maculatus by comparing female and male opportunity for selection (i) with and without limitation of quality oviposition sites, and (ii) under delayed age at oviposition. Decreasing the abundance of the resource key to females or increasing their reproductive age was challenging, as shown by a reduction in mean fitness, but opportunity for selection remained stronger in males across all treatments, and even more so when oviposition sites were limiting. This suggests that males remain the more variable sex independent of context, and that the opportunity for selection through males is indirectly affected by female-specific resource limitation.     

Experimental manipulation reveals differential effects of colour pattern on survival in male and female pygmy grasshoppers

Populations of pygmy grasshoppers, Tetrix subulata, exhibit genetically coded discontinuous variation in colour pattern. To determine whether the dynamics of this polymorphism is likely to be affected by selective processes, rather than by stochastic events, we experimentally manipulated colour patterns of free-ranging grasshoppers and then calculated and controlled for differences in capture probabilities between categories of individuals before estimating and testing for differences in survival using mark–recapture data and program SURGE . We found that paint treatment had a significant effect on survival, and that the relationship between colour pattern and survival was different in males and females. Our analyses also revealed significant differences between sexes in relative frequencies of natural colour morphs, body size, activity pattern, dispersal distance and microhabitat use. These findings accord with the hypothesis that colour pattern and behaviour jointly determine susceptibility to visual predators. Our data enable us to reject the null-hypothesis that colour pattern is a selectively neutral character and that the polymorphism is maintained solely by stochastic processes, such as random genetic drift and founder events. Indeed, the effect of dorsal coloration on survival, together with associations between colour pattern and many biologically important traits (body size, behaviour, thermal capacity, physiology and reproductive performance), suggests that colour pattern is likely to significantly influence individual fitness, and that the polymorphism must be maintained by some active process, such as spatially variable selection in combination with gene flow. The possible role of colour polymorphism as an intermediate stage in the evolution of sexual dichromatism in animals is discussed.     

Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman

Female choice and male-male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.     

Interactions among mechanisms of sexual selection on male body size and head shape in a sexually dimorphic fly

Abstract Darwin envisaged male-male and male-female interactions as mutually supporting mechanisms of sexual selection, in which the best armed males were also the most attractive to females. Although this belief continues to predominate today, it has been challenged by sexual conflict theory, which suggests that divergence in the interests of males and females may result in conflicting sexual selection. This raises the empirical question of how multiple mechanisms of sexual selection interact to shape targeted traits. We investigated sexual selection on male morphology in the sexually dimorphic fly Prochyliza xanthostoma , using indices of male performance in male-male and male-female interactions in laboratory arenas to calculate gradients of direct, linear selection on male body size and an index of head elongation. In male-male combat, the first interaction with a new opponent selected for large body size but reduced head elongation, whereas multiple interactions with the same opponent favored large body size only. In male-female interactions, females preferred males with relatively elongated heads, but male performance of the precopulatory leap favored large body size and, possibly, reduced head elongation. In addition, the amount of sperm transferred (much of which is ingested by females) was an increasing function of both body size and head elongation. Thus, whereas both male-male and male-female interactions favored large male body size, male head shape appeared to be subject to conflicting sexual selection. We argue that conflicting sexual selection may be a common result of divergence in the interests of the sexes.     

Models of clines in sexual selection by female choice

Most models of sexual selection by female choice have considered discrete, homogenous populations. This paper studies the evolution of a female preference along a cline in the frequency of a preferred male trait. Single alleles control both the preference and preferred character.
Fisher's process initially causes the preference to spread to some 'maximum' frequency with a corresponding rise in character gene frequency. At this stage, the cline in preference does not necessarily mirror that of the trait. Then, however, preference frequency usually decreases, albeit very slowly, and the preference cline always comes to mirror that of the preferred character. Eventually, preference is completely lost from the cline and the character cline decays to that seen under random mating. This loss can only be prevented if the preference is initially frequent enough to push the character to fixation throughout the cline.
Consequently, a preference that arises after the preferred trait may increase very little in frequency itself and have a negligible effect on trait frequency before being lost from the population. Special conditions, such as cyclical natural selection, may be necessary to explain the spread of a preference in a cline from a low initial frequency to frequencies as high as those observed. A preference that predates the preferred trait can enter the population at a high frequency and radically alter a cline in the frequency of a preferred male trait, albeit often transiently.     

Cryptic female preference for colorful males in guppies

Cryptic female choice (CFC) refers to female-mediated processes occurring during or after copulation that result in biased sperm use in favor of preferred or compatible males. Despite recent empirical support for this hypothesis, evidence that CFC contributes towards the evolution of male body ornaments, in the same way that precopulatory female choice does, is currently lacking. Here, we tested the possibility that CFC selects for increased male attractiveness in the guppy Poecilia reticulata, a freshwater fish exhibiting internal fertilization. Specifically, we examined whether females are able to manipulate the number of sperm transferred or retained at copulation in favor of relatively attractive males. In support of this prediction, we found that following solicited copulations the number of sperm inseminated is influenced exclusively by the female's perception of relative male coloration, independent of any direct manipulation of males themselves. Because females prefer brightly colored males during precopulatory mate choice, our finding that colorful males are also favored as a consequence of enhanced insemination success indicates that cryptic female choice can reinforce precopulatory preferences for extravagant male ornaments.