Nonlinear and correlational sexual selection on 'honest' female ornamentation

Female ornamentation has long been overlooked because of the greater prevalence of elaborate displays in males. However, the circumstances under which females would benefit from honestly signalling their quality are limited. Females are not expected to invest in ornamentation unless the fitness benefits of the ornament exceed those derived from investing the resources directly into offspring. It has been proposed that when females gain direct benefits from mating, females may instead be selected for ornamentation that deceives males about their reproductive state. In the empidid dance flies, males frequently provide nuptial gifts and it is usually only the female that is ornamented. Female traits in empidids, such as abdominal sacs and enlarged pinnate leg scales, have been proposed to 'deceive' males into matings by disguising egg maturity. We quantified sexual selection in the dance fly Rhamphomyia tarsata and found escalating, quadratic selection on pinnate scales and that pinnate scales honestly reflect female fecundity. Mated females had a larger total number and more mature eggs than unmated females, highlighting a potential benefit rather than a cost of male mate choice. We also show correlational selection on female pinnate scales and fecundity. Correlational selection, equivalent investment patterns or increased nutrition from nuptial gifts may all maintain honesty in female ornamentation.     

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.     

Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

A novel method of comparing mating success and survival reveals similar sexual and viability selection for mobility traits in female tree crickets

The relationship between sexual and viability selection in females is necessarily different than that in males, as investment in sexual traits potentially comes at the expense of both fecundity and survival. Accordingly, females do not usually invest in sexually selected traits. However, direct benefits obtained from mating, such as nuptial gifts, may encourage competition among females and subsidize investment into sexually selected traits. We compared sexual and viability selection on female tree crickets Oecanthus nigricornis, a species where females mate frequently to obtain nuptial gifts and sexual selection on females is likely. If male choice determines female mating success in this species, we expect sexual selection for fecundity traits, as males of many species prefer more fecund females. Alternatively, intrasexual scramble or combat competition on females may select for larger jumping legs or wider heads (respectively). We estimated mating success in wild caught crickets using microsatellite analysis of stored sperm and estimated relative viability by comparing surviving female O. nigricornis to those captured by a common wasp predator. In support of the scramble competition hypothesis, we found sexual selection for females with larger hind legs and narrower heads. We also found stabilizing viability selection for intermediate head width and hind leg size. As predicted, traits under viability and sexual selection were very similar, and the direction of that selection was not opposing. However, because the shape of sexual and viability selection differs, these episodes of selection may favour slightly different trait sizes.     

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load‐lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female‐specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load‐lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild‐caught male R. longicauda collected during copulation were experiencing load‐lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load‐lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.     

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.     

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.     

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.     

A test of the Darwin–Fisher theory for the evolution of male secondary sexual traits in monogamous birds

The Darwin–Fisher theory proposes that the presence of male secondary sexual traits in monogamous birds is selected for by early season breeding of females that are in good condition. These early breeding females have high fecundity because of their good condition, and they select mates based on secondary sex traits. We tested whether this hypothesis may be responsible for the presence of male sexual ornaments in the great frigatebird, a socially and genetically monogamous seabird. Consistent with the Darwin–Fisher theory, we found that reproductive success declined over the season. However, males with more exaggerated ornaments were not chosen as mates earlier in the season than males with less exaggerated ornaments, and selection gradients on these ornaments were not significantly different from zero.     

Can non‐directional male mating preferences facilitate honest female ornamentation?

Recent studies have demonstrated male mate choice for female ornaments in species without sex-role reversal. Despite these empirical findings, little is known about the adaptive dynamics of female signalling, in particular the evolution of male mating preferences. The evolution of traits that signal mate quality is more complex in females than in males because females usually provide the bulk of resources for the developing offspring. Here, we investigate the evolution of male mating preferences using a mathematical model which: (i) specifically accounts for the fact that females must trade-off resources invested in ornaments with reproduction; and (ii) allows male mating preferences to evolve a non-directional shape. The optimal adaptive strategy for males is to develop stabilizing mating preferences for female display traits to avoid females that either invests too many or too few resources in ornamentation. However, the evolutionary stability of this prediction is dependent upon the level of error made by females when allocating resources to either signal or fecundity.     

Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos

When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark-eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or "tail white") are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum-likelihood analysis of a long-term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male-male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.     

Contrasting patterns of selection on the size and coloration of a female plumage ornament in common yellowthroats

Females often possess ornaments that appear smaller and duller than homologous traits in males. These ornaments may arise as nonfunctional by‐products of sexual selection in males and cause negative viability or fecundity selection in females in proportion to the cost of their production and maintenance. Alternatively, female ornaments may function as signals of quality that are maintained by sexual or social selection. In a 4‐year study of 83 female common yellowthroats (Geothlypis trichas) and their 222 young, we found strong viability and fecundity selection on the yellow bib, a carotenoid‐based plumage ornament that is a target of sexual selection in males. Females with larger bibs were older, larger and more fecund than females with smaller bibs. However, bib size positively covaried with bib total brightness and carotenoid chroma, aspects of bib coloration that were under negative viability and fecundity selection. Females with more colourful bibs laid fewer eggs in their first clutch, were more likely to suffer total brood loss due to predation and were less likely to return to the study area. Selection against bib coloration limits the value of bib size as a quality indicator in females and may constrain the elaboration of bib attributes in males.     

Fecundity selection on ornamental plumage colour differs between ages and sexes and varies over small spatial scales

Avian plumage colours are some of the most conspicuous sexual ornaments, and yet standardized selection gradients for plumage colour have rarely been quantified. We examined patterns of fecundity selection on plumage colour in blue tits (Cyanistes caeruleus L.). When not accounting for environmental heterogeneity, we detected relatively few cases of selection. We found significant disruptive selection on adult male crown colour and yearling female chest colour and marginally nonsignificant positive linear selection on adult female crown colour. We discovered no new significant selection gradients with canonical rotation of the matrix of nonlinear selection. Next, using a long-term data set, we identified territory-level environmental variables that predicted fecundity to determine whether these variables influenced patterns of plumage selection. The first of these variables, the density of oaks within 50 m of the nest, influenced selection gradients only for yearling males. The second variable, an inverse function of nesting density, interacted with a subset of plumage selection gradients for yearling males and adult females, although the strength and direction of selection did not vary predictably with population density across these analyses. Overall, fecundity selection on plumage colour in blue tits appeared rare and inconsistent among sexes and age classes.     

Sexual selection resulting from extrapair paternity in collared flycatchers

Extrapair paternity has been suggested to represent a potentially important source of sexual selection on male secondary sexual characters, particularly in birds with predominantly socially monogamous mating systems. However, relatively few studies have demonstrated sexual selection within single species by this mechanism, and there have been few attempts to assess the importance of extrapair paternity in relation to other mechanisms of sexual selection. We report estimates of sexual selection gradients on male secondary sexual plumage characters resulting from extrapair paternity in the collared flycatcher Ficedula albicollis, and compare the importance of this form of sexual selection with that resulting from variation in mate fecundity. Microsatellite genotyping revealed that 15% of nestlings, distributed nonrandomly among 33% of broods (N=79), were the result of extrapair copulations. Multivariate selection analyses revealed significant positive directional sexual selection on two uncorrelated secondary sexual characters in males (forehead and wing patch size) when fledgling number was used as the measure of fitness. When number of offspring recruiting to the breeding population was used as the measure of male fitness, selection on these traits appeared to be directional and stabilizing, respectively. Pairwise comparisons of cuckolded and cuckolding males revealed that males that sired young through extrapair copulations had wider forehead patches, and were paired to females that bred earlier, than the males that they cuckolded. Path analysis was used to partition selection on these traits into pathways via mate fecundity and sperm competition, and suggested that the sperm competition pathway accounted for between 64 and 90% of the total sexual selection via the two paths. The selection revealed in these analyses is relatively weak in comparison with many other measures of selection in natural populations. We offer some explanations for the relatively weak selection detected. Copyright 1999 The Association for the Study of Animal Behaviour.     

Viability selection on female fly finery in the wild

Female ornaments have evolved in a few taxa in which females compete for access to important resources provided by their mates. However, the effects of these sexually selected traits on survival have not been studied. Elaborate leg‐scale and/or abdominal ornaments are displayed by females of some Rhamphomyia dance flies (Diptera: Empididae) to flying males carrying prey gifts (females do not hunt). Previous analyses have shown significant sexual selection on these female traits. We studied viability selection on the traits by sampling the webs of two spider species and comparing prey R. longicauda females to survivors. We also investigated viability selection from one of the spiders over two seasons. We found that the direction of viability selection on R. longicauda from sticky Tetragnatha spider webs was consistent over two seasons. For abdominal ornaments the form of viability selection was positive and primarily directional (linear). Viability selection also favoured shorter tibiae but there was no significant selection on the size of residual tibial scale area. However, with the addition of dance fly kills from the non‐sticky, leaf‐covering webs of a Dictyna spider, abundant in only one of the seasons, the overall direction of viability selection favoured larger tibial ornaments. While noting that this viability selection on tibial scale ornaments may be a statistical artefact of the fewer traits in the two‐predator analysis (abdominal structures were missing from most Dictyna prey), we suggest that simple differences in the natural history of selective agents causing mortality may partly explain the variation in whether sexual traits are under viability selection. Viability selection on ornamental traits may vary greatly between seasons with changes in the abundances of different natural enemies so that net directional selection on these traits over many generations may be weak.     

Ornaments or offspring: costs to reproductive success restrict sexual selection processes

If, in their partner choice, males seek direct benefits (fecund females), the result will be selection for traits indicating female quality rather than for arbitrary (Fisherian) traits. However, the costs of developing and maintaining the sexually selected traits (ornaments) may reduce the resources available to the female for allocation to reproduction and hence result in lower reproductive success per brood. This hitherto unrecognized fecundity cost of sexually selected traits will constrain both the potency of sexual selection mechanisms and the degree of elaboration of sexually selected traits in females, and can also apply to males which invest in their offspring: sexual selection becomes self-limiting. The fitness implications of these costs are examined for both sexes in a variety of mating and parental care patterns. Sexual selection acting on both sexes may lead to either dimorphism or monomorphism, the latter being the case when the quality indicators chosen by both sexes coincide. Ways of evasion or reduction of these reproductive costs of allocations to sexually selected traits include using different resource components for the ornament and for reproduction, or partitioning the two allocations in time.     

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

Evolution of animal genitalia: morphological correlates of fitness components in a water strider

Rapid divergence of male genitalia is one of the most general evolutionary trends in animals with internal fertilization, but the mechanisms of genital evolution are poorly understood. The current study represents the first comprehensive attempt to test the main hypotheses that have been suggested to account for genital evolution (the lock-and-key, sexual selection and pleiotropy hypotheses) with intraspecific data. We measure multivariate phenotypic selection in a water strider species, by relating five different components of fitness (mating frequency, fecundity, egg hatching rate, offspring survival rate and offspring growth rate) to a suite of genital and non-genital morphological traits (in total 48). Body size had a series of direct effects in both sexes. Large size in females was positively related to both fecundity and egg hatching rate. There was positive sexual selection for large size in males (mating frequency), which to some extent was offset by a reduced number of eggs laid by females mated to large males. Male genitalic morphology influenced male mating frequency, but the detected directional selection on genitalia was due to indirect selection on phenotypically correlated non-intromittent traits. Further, we found no assortative mating between male intromittent genitalia and female morphology. Neither did we find any indications of male genitalia conveying information of male genetic quality. Several new insights can be gained from our study. Most importantly, our results are in stark disagreement with the long standing lock-and-key hypothesis of genital evolution, as well as with certain models of sexual selection. Our results are, however, in agreement with other models of sexual selection as well as with the pleiotropy hypothesis of genital evolution. Fluctuating asymmetry of bilaterally symmetrical traits, genital as well as non-genital, had few effects on fitness. Females with low fluctuating asymmetry in leg length produced offspring with a higher survival rate, a pattern most proba bly caused by direct phenotypic maternal effects. We also discuss the relevance of our results to sexual conflict over mating, and the evolution of sexual traits by coevolutionary arms races between the sexes.     

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.     

Female‐biased size dimorphism in a diapausing caddisfly,Mesophylax aspersus: effect of fecundity and natural and sexual selection

1. The effect of mating success, female fecundity and survival probability associated with intra‐sex variation in body size was studied in Mesophylax aspersus, a caddisfly species with female‐biased sexual size dimorphism, which inhabits temporary streams and aestivates in caves. Adults of this species do not feed and females have to mature eggs during aestivation. 2. Thus, females of larger size should have a fitness advantage because they can harbour more energy reserves that could influence fecundity and probability of survival until reproduction. In contrast, males of smaller size might have competitive advantages over others in mating success. 3. These hypotheses were tested by comparing the sex ratio and body size of individuals captured before and after the aestivation period. The associations between body size and female fecundity, and between mating success and body size of males, were explored under laboratory conditions. 4. During the aestivation period, the sex ratio changed from 1 : 1 to male biased (4 : 1), and a directional selection on body size was detected for females but not for males. Moreover, larger clutches were laid by females of larger size. Finally, differences in mating success between small and large males were not detected. These results suggest that natural selection (i.e. the differential mortality of females associated with body size) together with possible fecundity advantages, are important factors responsible of the sexual size dimorphism of M. aspersus. 5. These results highlight the importance of taking into account mechanisms other than those traditionally used to explain sexual dimorphism. Natural selection acting on sources of variation, such as survival, may be as important as fecundity and sexual selection in driving the evolution of sexual size dimorphism.