Sexually selected dichromatism in the hihi Notiomystis cincta: multiple colours for multiple receivers

Why do some bird species show dramatic sexual dichromatism in their plumage? Sexual selection is the most common answer to this question. However, other competing explanations mean it is unwise to assume that all sexual dichromatism has evolved by this mechanism. Even if sexual selection is involved, further work is necessary to determine whether dichromatism results from competition amongst rival males, or by female choice for attractive traits, or both. Here, we test whether sexually dichromatic hihi (Notiomystis cincta) plumage is currently under sexual selection, with detailed behavioural and genetic analyses of a free‐living island population. Bateman gradients measured for males and females reveal the potential for sexual selection, whilst selection gradients, relating reproductive success to specific colourful traits, show that there is stabilizing selection on white ear tuft length in males. By correlating colourful male plumage with different components of reproductive success, we show that properties of yellow plumage are most likely a product of male–male competition, whilst properties of the black and white plumage are an outcome of both male–male competition and female choice. Male plumage therefore potentially signals to multiple receivers (rival males and potential mates), and this may explain the multicoloured appearance of one of the most strikingly dichromatic species in New Zealand.     

Sexually antagonistic association between paternal phenotype and offspring viability reinforces total selection on a sexually selected trait

The evolution of conspicuous sexually selected traits, such as horns or antlers, has fascinated biologists for more than a century. Elaborate traits can only evolve if they substantially increase reproduction, because they probably incur survival costs to the bearer. Total selection on these traits, however, includes sexual selection on sires and viability selection on offspring and can be influenced by changes in each of these components. Non-random associations between paternal phenotype and offspring viability may thus affect total selection on sexually selected traits. Long-term data on wild bighorn sheep (Ovis canadensis) provide the first evidence in nature that association between paternal phenotype and lamb viability strengthens total selection on horn size of adult rams, a sexually selected trait. The association of paternal horn length and offspring viability was sexually antagonistic: long-horned males sired sons with high viability but daughters of low viability. These results shed new light on the evolutionary dynamics of an iconic sexually selected trait and have important implications for sustainable wildlife management.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.     

Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite

Elaborate sexually selected ornaments and armaments are costly but increase the reproductive success of their bearers (usually males). It has been postulated that high-quality males can invest disproportionately more in such traits, making those traits honest signals of genetic quality. However, genes associated with such traits may have sexually antagonistic effects on fitness. Here, using a bulb mite Rhizoglyphus robini, a species in which a distinct dimorphism exists between males in the expression of a sexually selected weapon, we compare inbreeding and gender load between lines derived from armed fighters and unarmed scramblers. After four generations of sib-mating, inbreeding depression for female fitness was significantly lower in fighter-derived lines compared to scrambler-derived lines, suggesting that fighter males had significantly higher genetic quality. However, outbred females from fighter-derived lines had significantly lower fitness compared to outbred females from scrambler-derived lines, demonstrating significant gender load associated with the presence of a sexually selected male weapon. Our results imply that under outbreeding, genetic benefits of mating with bearers of elaborate sexually selected traits might be swamped by the costs of decreased fitness of female progeny due to sexually antagonistic effects.     

Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers

The response to intradermally injected phytohaemagglutinin (PHA-response) is a commonly used quantification of avian immunocompetence (the ability to resist pathogens). Parasite-mediated sexual selection requires heritable immunocompetence, but evidence for heritability of PHA-response in birds largely stems from full-sib comparisons. Using an animal model approach, we quantified the narrow-sense heritability of PHA-response in 1626 collared flycatcher (Ficedula albicollis) nestlings from 332 families, most of which were cross-fostered. Nestling PHA-response was not significantly heritable (h2=0.06+/-0.10), but was subject to non-heritable nest-of-origin effects (10% of variation). Our findings illustrate that full-sib comparisons of immunological measures may lead to an inflated estimate of heritability and also reveal a limited role of nestling PHA-response for sexual selection in this population.     

Corticosterone regulates multiple colour traits in Lacerta [Zootoca] vivipara males

Ornamental colours usually evolve as honest signals of quality, which is supported by the fact that they frequently depend on individual condition. It has generally been suggested that some, but not all types of ornamental colours are condition dependent, indicating that different evolutionary mechanisms underlie the evolution of multiple types of ornamental colours even when these are exhibited by the same species. Stress hormones, which negatively affect condition, have been shown to affect colour traits based on different pigments and structures, suggesting that they mediate condition dependence of multiple ornament types both among and within individuals. However, studies investigating effects of stress hormones on different ornament types within individuals are lacking, and thus, evidence for this hypothesis is scant. Here, we investigated whether corticosterone mediates condition dependence of multiple ornaments by manipulating corticosterone levels and body condition (via food availability) using a two‐factorial design and by assessing their effect on multiple colour traits in male common lizards. Corticosterone negatively affected ventral melanin‐ and carotenoid‐based coloration, whereas food availability did not affect coloration, despite its significant effect on body condition. The corticosterone effect on melanin‐ and carotenoid‐based coloration demonstrates the condition dependence of both ornaments. Moreover, corticosterone affected ventral coloration and had no effect on the nonsexually selected dorsal coloration, showing specific effects of corticosterone on ornamental ventral colours. This suggests that corticosterone simultaneously mediates condition dependence of multiple colour traits and that it therefore accounts for covariation among them, which may influence their evolution via correlational selection.     

Courtship song and immune function in the field cricket Gryllus bimaculatus

It has been assumed that sexual ornaments have evolved to reveal males' health and vigour for females. Choosy females may indirectly use ornaments as an indicator of the presence and effectiveness of genes for resistance against parasites. In this study we tested whether females of the Mediterranean field cricket, Gryllus bimaculatus, can use courtship song as a cue for choosing males with high immunocompetence, measured as encapsulation rate of nylon implants and lytic activity of haemolymph. We found that female crickets preferred courtship songs from males with a high encapsulation rate. Female crickets also had a tendency to prefer courtship songs with high tick rate and long high-frequency tick duration. These preferred song components were positively correlated with encapsulation rate, but negatively correlated with lytic activity of the male. In contrast to previous studies of crickets, there was no correlation between male weight and encapsulation rate or lytic activity. There is some evidence in another cricket species that the ability to encapsulate pathogens is heritable. Thus, in light of this study it seems possible that by preferring males according to their courtship song, females might benefit by increasing the parasite resistance of their offspring.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 503–510.     

Tail length in birds in relation to tail shape,general flight ecology and sexual selection

Relative tail length (longtailedness) of Palearctic birds was assessed by the standardized residuals of log–log regressions of tail length on wing length and tarsus length. The mean degree of tail shortening was greater than mean degree of tail lengthening, but there was a greater frequency of extreme long-tailed than short-tailed species. Longtailedness was greater in ornamental pin, lyre, deep forked and graduated shaped tails. These shapes (except graduated, for which data were lacking) were also relatively long-tailed according to shortest-rectrix lengths, this extra length potentially contributing compensatory lift. In forked tails, tail ratio increased linearly with longtailedness to above the aerodynamic optimum, and thus the most elongated forked tails were also more deeply forked. Tail shortening was marked for rounded tails, a surprising result in view of their slightly ornamental shape. Phylogenetically independent contrasts showed significantly greater longtailedness in graduated than square-tailed species, confirming the species-wide analysis. In phylogenetically independent contrasts of longtailedness and ecological factors, short-tailed species had significantly greater flight distances than medium-tailed species, but long- and medium-tailed species did not differ in migratory distance, foraging distance, overall flight distance or importance of aerial foraging. The data suggest that ecological factors, i.e. natural selection, are more important in the evolution of short-tailedness than longtailedness in birds, and that an additional influence of sexual selection on tail length and shape is also widespread.     

Sexually selected traits are larger and more variable in male than female beach-spawning capelin,Mallotus villosus

We evaluated whether morphological traits in capelin, Mallotus villosus, that appear to be sexually selected (pectoral fin, pelvic fin, anal fin, lateral ridge) were larger and more variable in males than females compared with naturally selected morphological traits (eyes, dorsal fin). Photographs were obtained of 136 capelin captured at two spawning sites and standardised measurements were taken of six morphological traits. Males had larger traits than females for a given body size and this was most pronounced in the traits thought to be sexually selected. Body size explained much of the variation in female traits but less variation in male traits, suggesting alternative selection pressures are involved. We suggest that larger male body size aids in endurance rivalry and sexually dimorphic traits help males to remain in physical contact with females while spawning on the beach.     

Sexually antagonistic coevolution in insects is associated with only limited morphological diversity

Morphological traits involved in male-female sexual interactions, such as male genitalia, often show rapid divergent evolution. This widespread evolutionary pattern could result from sustained sexually antagonistic coevolution, or from other types of selection such as female choice or selection for species isolation. I reviewed the extensive but under-utilized taxonomic literature on a selected subset of insects, in which male-female conflict has apparently resulted in antagonistic coevolution in males and females. I checked the sexual morphology of groups comprising 500-1000 species in six orders for three evolutionary trends predicted by the sexually antagonistic coevolution hypothesis: males with species-specific differences and elaborate morphology in structures that grasp or perforate females in sexual contexts; corresponding female structures with apparently coevolved species-specific morphology; and potentially defensive designs of female morphology. The expectation was that the predictions were especially likely to be fulfilled in these groups. A largely qualitative overview revealed several surprising patterns: sexually antagonistic coevolution is associated with frequent, relatively weak species-specific differences in males, but male designs are usually relatively simple and conservative (in contrast to the diverse and elaborate designs common in male structures specialized to contact and hold females in other species, and also in weapons such as horns and pincers used in intra-specific battles); coevolutionary divergence of females is not common; and defensive female divergence is very uncommon. No cases were found of female defensive devices that can be facultatively deployed. Coevolutionary morphological races may have occurred between males and females of some bugs with traumatic insemination, but apparently as a result of female attempts to control fertilization, rather than to reduce the physical damage and infections resulting from insertion of the male's hypodermic genitalia. In sum, the sexually antagonistic coevolution that probably occurs in these groups has generally not resulted in rapid, sustained evolutionary divergence in male and female external sexual morphology. Several limitations of this study, and directions for further analyses are discussed.     

The allometry between secondary sexual traits and body size is nonlinear among cervids

Allometric relationships between sexually selected traits and body size have been extensively studied in recent decades. While sexually selected traits generally display positive allometry, a few recent reports have suggested that allometric relationships are not always linear. In male cervids, having both long antlers and large size provides benefits in terms of increased mating success. However, such attributes are costly to grow and maintain, and these costs might constrain antler length from increasing at the same rate as body mass in larger species if the quantity of energy that males can extract from their environment is limiting. We tested for possible nonlinearity in the relationship between antler size and body mass (on a log–log scale) among 31 cervids and found clear deviation from linearity in the allometry of antler length. Antler length increased linearly until a male body mass threshold at approximately 110 kg. Beyond this threshold, antler length did not change with increasing mass. We discuss this evidence of nonlinear allometry in the light of life-history theory and stress the importance of testing for nonlinearity when studying allometric relationships.     

Multivariate selection and intersexual genetic constraints in a wild bird population

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra‐ and intersex additive genetic (co)variances and sex‐specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex‐specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex‐specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross‐sex genetic correlation = ?0.003, 95% CI = ?0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex‐specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.     

MHC,mate choice and heterozygote advantage in a wild social primate

Preferences for mates carrying dissimilar genes at the major histocompatibility complex (MHC) may help animals increase offspring pathogen resistance or avoid inbreeding. Such preferences have been reported across a range of vertebrates, but have rarely been investigated in social species other than humans. We investigated mate choice and MHC dynamics in wild baboons (Papio ursinus). MHC Class II DRB genes and 16 microsatellite loci were genotyped across six groups (199 individuals). Based on the survey of a key segment of the gene‐rich MHC, we found no evidence of mate choice for MHC dissimilarity, diversity or rare MHC genotypes. First, MHC dissimilarity did not differ from random expectation either between parents of the same offspring or between immigrant males and females from the same troop. Second, female reproductive success was not influenced by MHC diversity or genotype frequency. Third, population genetic structure analysis revealed equally high genotypic differentiation among troops, and comparable excess heterozygosity within troops for juveniles, at both Mhc‐DRB and neutral loci. Nevertheless, the age structure of Mhc‐DRB heterozygosity suggested higher longevity for heterozygotes, which should favour preferences for MHC dissimilarity. We propose that high levels of within‐group outbreeding, resulting from group‐living and sex‐biased dispersal, might weaken selection for MHC‐disassortative mate choice.     

Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations

Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signalling axes, despite very low‐level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely related wild populations.     

Predation selects for increased immune function in male damselflies, Calopteryx splendens

Predation selects for numerous traits in many animal species, with sick or parasitized prey often being at high risk. When challenged by parasites and pathogens, prey with poor immune functions are thus likely to be at a selective disadvantage. We tested the hypothesis that predation by birds selects for increased immune function in a wild population of male damselflies Calopteryx splendens, while controlling for a trait known to be under selection by bird predation, dark wing-spots. We found that selection on both immune function and wing-spot size was significantly positive, and that selection on either trait was independent of selection on the other. We found no evidence of nonlinear quadratic or correlational selection. In contrast to previous studies, we found no phenotypic correlation between immune function and wing-spot size. There was also no difference in immune response between territorial and non-territorial males. Our study suggests that predation may be an important agent of selection on the immune systems of prey, and because the selection we detected was directional, has the potential to cause phenotypic change in populations.     

Seasonal colour change by moult or by the abrasion of feather tips: a comparative study

Many birds undergo seasonal changes in plumage coloration by prebreeding moult, abrasion of cryptic feather tips, or both. Seasonal dichromatism is thought to result from optimizing coloration to the conflicting demands of different life-cycle periods, sexual selection for conspicuousness being substantial during the mating season, whereas selection for camouflage and for social signals may act in all seasons. Furthermore, energetic and time demands may constrain the extent of moult, thereby limiting colour change. We investigated the relative importance of several factors in shaping this variation in a songbird clade using phylogenetic comparative methods. We found that prebreeding moult relates most strongly to breeding onset and winter diet, demonstrating that both time and food availability constrain feather replacement. Feather abrasion was best predicted by winter flocking behaviour, and secondarily by open habitats, implying that exposure to predators and the simultaneous need for social signalling may favour the expression of partially obscured ornaments in the non-breeding season. The combined occurrence of prebreeding moult and feather abrasion was associated with the polygynous mating system, suggesting that species under strong sexual selection may employ both strategies of colour change to ensure the full expression of breeding coloration.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 711–721.     

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

Major histocompatibility complex (MHC)‐associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC‐associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC‐dependent mate choice occurs across the order in a variety of socio‐sexual systems and favours mates with dissimilar, diverse or specific genotypes non‐exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.