Extra-pair paternity and sexual dimorphism in birds

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.     

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.     

Reversed plumage ontogeny in a female hummingbird: implications for the evolution of iridescent colours and sexual dichromatism

In polygynous birds, bright plumage is typically more extensive in the sexually competitive males and develops at or after sexual maturity. These patterns, coupled with the importance of male plumage in sexual displays, fostered the traditional hypothesis that bright plumages and sexual dichromatism develop through the actions of sexual selection on males. This view remains problematic for hummingbirds, all of which are polygynous, because their bright iridescent plumages are also important non-sexual signals associated with dominance at floral nectar sources. Here I show that female amethyst-throated sunangels [ Heliangelus amethysticollis (d'Orbigny & Lafresnaye)], moult from an immature plumage with an iridescent gorget to an adult plumage with a non-iridescent gorget. This 'reversed' ontogeny contradicts the notion that iridescent plumage has a sexual function because sexual selection in polygynous birds should be lowest among non-reproductive immature females. Moreover, loss of iridescent plumage in adult females indicates that adult sexual dichromatism in H. amethysticollis is due in large part to changes in female ontogeny. I suggest that both the ontogeny and sexual dichromatism evolved in response to competition for nectar.     

Migration and the evolution of sexual dichromatism: evolutionary loss of female coloration with migration among wood-warblers

The mechanisms underlying evolutionary changes in sexual dimorphism have long been of interest to biologists. A striking gradient in sexual dichromatism exists among songbirds in North America, including the wood-warblers (Parulidae): males are generally more colourful than females at northern latitudes, while the sexes are similarly ornamented at lower latitudes. We use phylogenetically controlled comparative analysis to test three non-mutually exclusive hypotheses for the evolution of sexual dichromatism among wood-warblers. The first two hypotheses focus on the loss of female coloration with the evolution of migration, either owing to the costs imposed by visual predators during migration, or owing to the relaxation of selection for female social signalling at higher latitudes. The third hypothesis focuses on whether sexual dichromatism evolved owing to changes in male ornamentation as the strength of sexual selection increases with breeding latitude. To test these hypotheses, we compared sexual dichromatism to three variables: the presence of migration, migration distance, and breeding latitude. We found that the presence of migration and migration distance were both positively correlated with sexual dichromatism, but models including breeding latitude alone were not strongly supported. Ancestral state reconstruction supports the hypothesis that the ancestral wood-warblers were monochromatic, with both colourful males and females. Combined, these results are consistent with the hypotheses that the evolution of migration is associated with the relaxation of selection for social signalling among females and that there are increased predatory costs along longer migratory routes for colourful females. These results suggest that loss of female ornamentation can be a driver of sexual dichromatism and that social or natural selection may be a stronger contributor to variation in dichromatism than sexual selection.     

Evolution of sexual dichromatism in relation to nesting habits in European passerines: a test of Wallace's hypothesis

Wallace proposed in 1868 that natural rather than sexual selection could explain the striking differences in avian plumage dichromatism. Thus, he predicted that nesting habits, through their association with nest predation, could drive changes in sexual dichromatism by enabling females in cavity nesters to become as conspicuous as males, whereas Darwin (1871, The Descent of Man and Selection in Relation to Sex, John Murray, London) argued that sexual selection was the sole explanation for dichromatism. Sexual dichromatism is currently used as indicating the strength of sexual selection, and therefore testing Wallace's claim with modern phylogentically controlled methodologies is of prime interest for comparing the roles of natural and sexual selection in affecting the evolution of avian coloration. Here, we have related information on nest attendance, sexual dichromatism and nesting habits (open and cavity nesting) to male and female plumage conspicuousness in European passerines. Nest incubation attendance does not explain male or female plumage conspicuousness but nest type does. Moreover, although females of monochromatic and cavity nesting species are more conspicuous than females of other species, males of monochromatic and open nesting species are those with more cryptic plumage. Finally, analyses of character evolution suggest that changes in nesting habits influence the probability of changes in both dichromatism and plumage conspicuousness of males but do not significantly affect those in females. These results strongly suggest a role of nesting habits in the evolution of plumage conspicuousness of males, and a role for sexual selection also in females, both factors affecting the evolution of sexual dichromatism. We discuss our findings in relation to the debate that Darwin and Wallace maintained more than one century ago on the importance of natural and sexual selection in driving the evolution of plumage conspicuousness and sexual dichromatism in birds, and conclude that our results partly support the evolutionary scenarios envisaged by both extraordinary scientists.     

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.     

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.     

Sexual Selection on male cuticular hydrocarbons via male–male competition and female choice

Traditional views of sexual selection assumed that male–male competition and female mate choice work in harmony, selecting upon the same traits in the same direction. However, we now know that this is not always the case and that these two mechanisms often impose conflicting selection on male sexual traits. Cuticular hydrocarbons (CHCs) have been shown to be linked to both social dominance and male attractiveness in several insect species. However, although several studies have estimated the strength and form of sexual selection imposed on male CHCs by female mate choice, none have established whether these chemical traits are also subject to sexual selection via male–male competition. Using a multivariate selection analysis, we estimate and compare sexual selection exerted by male–male competition and female mate choice on male CHC composition in the broad‐horned flour beetle Gnatocerus cornutus. We show that male–male competition exerts strong linear selection on both overall CHC abundance and body size in males, while female mate choice exerts a mixture of linear and nonlinear selection, targeting not just the overall amount of CHCs expressed but the relative abundance of specific hydrocarbons as well. We discuss the potential implications of this antagonistic selection with regard to male reproductive success.     

Song post exposure, song features, and predation risk

Male birds use song to attract mates and deter other males,but in doing so, they also attract the attention of predatorsand parasites. Such viability costs are inherent in reliablesignals, potentially causing females to prefer mates that displayfrom the most exposed sites. However, viability costs of sexualsignals may be ameliorated by affecting the choice of microhabitat,which in turn may affect the design of song features that aremost efficiently transmitted in this microhabitat. We estimatedthe exposure of song posts (microsites used by males when singing)used by passerine birds in relation to prey selection by thesparrowhawk Accipiter nisus, by calculating the proportion ofmales that sang from song posts that were at the maximum levelof the vegetation, in an attempt to quantify the costs of sexualselection. We quantified prey susceptibility to predation asthe difference between the log-transformed observed number ofprey minus the log-transformed expected number of prey in theenvironment. This prey susceptibility index increased with increasingsong post exposure similarly in sexually dichromatic and monochromaticspecies, although the prey susceptibility index was relatedto sexual dichromatism. Song post exposure was dependent onhabitat, but comparative models controlling for the potentiallyconfounding effects of habitat, sexual dichromatism, hole nesting,coloniality, body mass, cognitive capacities, and flying abilitiesindicated that the relationship between the prey susceptibilityindex and song post exposure is strong. Path analyses of therelationship between song post exposure, sexual dichromatism,and prey susceptibility index revealed that selection actingon sexual dichromatism and song post exposure has secondaryimpact on prey susceptibility index. The opposite causal mechanismsby which predation affects sexual traits are less likely. Thesemodels suggest that female preference for high song posts ordichromatic plumage increases predation risk on an evolutionarytime scale.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

Intrasexual competition underlies sexual selection on male breeding coloration in the orangethroat darter,Etheostoma spectabile

Elaborate, sexually dimorphic traits are widely thought to evolve under sexual selection through female preference, male–male competition, or both. The orangethroat darter (Etheostoma spectabile) is a sexually dichromatic fish in which females exhibit no preferences for male size or coloration. We tested whether these traits affect individual reproductive success in E. spectabile when multiple males are allowed to freely compete for a female. The quality and quantity of male coloration were associated with greater success in maintaining access to the female and in spawning as the primary male (first male to participate). On the other hand, sneaking behavior showed little correlation with coloration. Male breeding coloration in E. spectabile may therefore demonstrate how intrasexual competition can be a predominant factor underlying the evolution of male ornaments.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Using photogrammetry and color scoring to assess sexual dimorphism in wild western gorillas (Gorilla gorilla)

Investigating sexual dimorphism is important for our understanding of its influence on reproductive strategies including male-male competition, mate choice, and sexual conflict. Measuring physical traits in wild animals can be logistically challenging and disruptive for the animals. Therefore body size and ornament variation in wild primates have rarely been quantified. Gorillas are amongst the most sexually dimorphic and dichromatic primates. Adult males (silverbacks) possess a prominent sagittal crest, a pad of fibrous and fatty tissue on top of the head, have red crest coloration, their saddle appears silver, and they possess a silverline along their stomach. Here we measure levels of sexual dimorphism and within-male variation of body length, head size, and sexual dichromatism in a population of wild western gorillas using photogrammetry. Digital photogrammetry is a useful and precise method to measure sexual dimorphism in physical traits yielding sexual dimorphism indices (ISD), similar to those derived from traditional measurements of skeletal remains. Silverbacks were on an average 1.23 times longer in body length than adult females. Sexual dimorphism of head size was highest in measures of crest size (max ISD: 60.4) compared with measures of facial height (max ISD: 24.7). The most sexually dimorphic head size measures also showed the highest within-sex variation. We found no clear sex differences in crest coloration but there was large sexual dichromatism with high within-male variation in saddle coloration and silverline size. Further studies should examine if these sexually dimorphic traits are honest signals of competitive ability and confer an advantage in reproductive success.     

RECONSTRUCTING THE EVOLUTION OF SEXUAL DICHROMATISM: CURRENT COLOR DIVERSITY DOES NOT REFLECT PAST RATES OF MALE AND FEMALE CHANGE

Males of sexually dimorphic species often appear more divergent among taxa than do females, so it is often assumed that evolutionary changes have occurred primarily in males. Yet, sexual dimorphisms can result from historical changes in either or both of the sexes, and few previous studies have investigated such patterns using phylogenetic methods. Here, we describe the evolution of male and female plumage colors in the grackles and allies (Icteridae), a songbird clade with a broad range in levels of sexual dichromatism. Using a model of avian perceptual color space, we calculated color distances within and among taxa on a molecular phylogeny. Our results show that female plumage colors have changed more dramatically than male colors in the evolutionary past, yet male colors are significantly more divergent among species today. Historical increases in dichromatism have involved changes in both sexes, whereas decreases in dichromatism have nearly always involved females evolving rapidly to look like males. Dichromatism is also associated with mating system in this group, with monogamous taxa tending to exhibit relatively low levels of sexual dichromatism. Our findings suggest that, despite appearances, female plumage evolution plays a more prominent role in sexual dichromatism than is generally assumed.     

Male courtship attractiveness and paternity success in Photinus greeni fireflies

Although female mate choice and male sperm competition have separately attracted much attention, few studies have addressed how precopulatory and postcopulatory episodes of sexual selection might interact to drive the evolution of male traits. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, and females gain direct benefits through male nuptial gifts acquired during multiple matings over several nights. We experimentally manipulated matings of P. greeni fireflies to test the hypothesis that postcopulatory paternity success might be biased toward males that are more attractive during courtship interactions. We first measured male courtship attractiveness to individual females using field behavioral assays. Females were then assigned to two double-mating treatments: (1) least attractive second male-females were first mated with their most attractive male, followed by their least attractive male, or (2) most attractive second male-females mated with males in reverse order. Larval offspring produced by each female following these double matings were genotyped using random amplified polymorphic DNA (RAPD) markers, and male paternity was determined. Contrary to prediction, firefly males that were more attractive to females based on their bioluminescent courtship displays subsequently showed significantly lower paternity, reflecting possible male trade-offs or sexual conflict. Differences in male paternity were not related to male body condition, testes or accessory gland mass, or to variation in female spermathecal size. Additionally, this study suggests that changes in phenotypic selection gradients may occur during different reproductive stages. These results indicate that it is crucial for future studies on sexual selection in polyandrous species to integrate both precopulatory and postcopulatory episodes to fully understand the evolution of male traits.     

The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae)

Males and females can be under different evolutionary pressures if sexual and natural selection is differentially operating in each sex. As a result, many species have evolved sexual dichromatism, or differences in coloration between sexes. Although sexual dichromatism is often used as an index of the magnitude of sexual selection, sexual dichromatism is a composite trait. Here, we examine the evolution of sexual dichromatism in one of the largest and most ecologically diverse families of birds, the tanagers, using the avian visual perspective and a species‐level phylogeny. Our results demonstrate that the evolutionary decreases of sexual dichromatism are more often associated with larger and more frequent changes in male plumage coloration, and evolutionary increases are not more often associated with larger changes in either sex. Furthermore, we show that the crown and ventral plumage regions are correlated with sexual dichromatism in males, and that only male plumage complexity is positively correlated with sexual dichromatism. Finally, we demonstrate that light environment is important in shaping both plumage brilliance and complexity. By conducting a multilevel analysis of plumage evolution in males and females, we show that sexual dichromatism evolves via a mosaic of sexual and natural selection in both sexes.     

Male Red-winged Blackbirds with experimentally dulled epaulets experience no disadvantage in sexual selection

ABSTRACT.   The epaulets of male Red-winged Blackbirds ( Agelaius phoeniceus ) are frequently cited as a sexually selected plumage ornament, but a number of laboratory and field studies provide little evidence that they are currently experiencing sexual selection. We used hair dye to dull epaulets of free-living territorial males prior to pair formation to determine if manipulated males experienced disadvantages in comparison with control males. We found no differences between control males and males with dulled epaulets in territorial behavior (territory size, song rate, trespass rate, and loss of territory), paternal care (time spent on territory and in antipredator sentinel behavior, and response to a model crow to simulate the threat of predation), pairing success (number of social mates), apparent reproductive success (numbers of nesting attempts, eggs/nest, nestlings/egg, and fledglings/nestling), or realized reproductive success (numbers of within-pair, extra-pair, and total fledglings as determined by DNA fingerprinting). We then used a meta-analysis of 11 published studies of Red-winged Blackbirds to determine if there is an overall effect of epaulet color or size on male-male competition, female choice, or reproductive success. Our results show that epaulet size has a small positive effect on male reproductive success, but epaulet color has no effect on male-male competition, female choice, and male reproductive success. One explanation for the seeming contradiction between studies that show that epaulets are necessary for territory defense and those that conclude that epaulets are not currently under selection is that epaulets serve as one of several cues of species recognition, especially among males at close range. An alternative explanation proposes counter-balancing intersexual advantages and intrasexual disadvantages of epaulet expression. Additional studies are needed to test these alternatives.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Colourful male European Serins Serinus serinus are more careful with their plumage

Ornamental traits typically advertise individual condition and can be costly to maintain. Plumage maintenance behaviour can increase plumage quality and positively influence female mate preference. We investigated this prediction by performing female mate‐choice trials and measuring male plumage maintenance behaviour in the European Serin Serinus serinus. More colourful males spent more time in plumage maintenance than less colourful males, but this was not correlated with body condition or ectoparasite load. Females preferred more colourful males, although this was not influenced by male plumage maintenance. Our findings highlight the fact that investment in plumage maintenance depends on individual coloration and this may reinforce the honesty of ornamental plumage and convey positive information for mate choice.