The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae)

Closely related animal lineages often vary in male coloration, and ecological selection is hypothesized to shape this variation. The role of ecological selection in inhibiting male color has been documented extensively at the population level, but relatively few studies have investigated the evolution of male coloration across a clade of closely related species. Darters are a diverse group of fishes that vary in the presence of elaborate male nuptial coloration, with some species exhibiting vivid color patterns and others mostly or entirely achromatic. We used phylogenetic logistic regression to test for correlations between the presence/absence of color traits across darter species and the ecological conditions in which these species occur. Environmental variables were correlated with the presence of nuptial color in darters with colorful species tending to inhabit environments that would support fewer predators and potentially transmit a broader spectrum of natural light compared to species lacking male coloration. We also tested the color preferences of a common darter predator, largemouth bass, and found that it exhibits a strong preference for red, providing further evidence of predation as a source of selection on color evolution in darters. Ecological selection therefore appears to be an important factor in dictating the presence or absence of male coloration in this group of fishes.     

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.     

Changes in sexual signals are greater than changes in ecological traits in a dichromatic group of fishes

Understanding the mechanisms by which phenotypic divergence occurs is central to speciation research. These mechanisms can be revealed by measuring differences in traits that are subject to different selection pressures; greater influence of different types of selection can be inferred from greater divergence in associated traits. Here, we address the potential roles of natural and sexual selection in promoting phenotypic divergence between species of snubnose darters by comparing differences in body shape, an ecologically relevant trait, and male color, a sexual signal. Body shape was measured using geometric morphometrics, and male color was measured using digital photography and visual system‐dependent color values. Differences in male color are larger than differences in body shape across eight allopatric, phylogenetically independent species pairs. While this does not exclude the action of divergent natural selection, our results suggest a relatively more important role for sexual selection in promoting recent divergence in darters. Variation in the relative differences between male color and body shape across species pairs reflects the continuous nature of speciation mechanisms, ranging from ecological speciation to speciation by sexual selection alone.     

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.     

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.     

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.     

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.     

Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards

Both sexual selection and natural selection can influence the form of dimorphism in secondary sexual traits. Here, we used a comparative approach to examine the relative roles of sexual selection and natural selection in the evolution of sexually dimorphic coloration (dichromatism) and ornamentation in agamid lizards. Sexual dimorphism in head and body size were used as indirect indicators of sexual selection, and habitat type (openness) as an index of natural selection. We examined separately the dichromatism of body regions "exposed to" and "concealed from" visual predators, because these body regions are likely to be subject to different selection pressures. Dichromatism of "exposed" body regions was significantly associated with habitat type: males were typically more conspicuously coloured than females in closed habitats. By contrast, dichromatism of "concealed" body regions and ornament dimorphism were positively associated with sexual size dimorphism (SSD). When we examined male and female ornamentation separately, however, both were positively associated with habitat openness in addition to snout-vent length and head SSD. These results suggest that natural selection constrains the evolution of elaborate ornamentation in both sexes as well as sexual dichromatism of body regions exposed to visual predators. By contrast, dichromatism of "concealed" body regions and degree of ornament dimorphism appear to be driven to a greater degree by sexual selection.     

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.     

A PHYLOGENETIC PERSPECTIVE ON THE EVOLUTION OF SEXUAL DICHROMATISM IN TANAGERS (THRAUPIDAE): THE ROLE OF FEMALE VERSUS MALE PLUMAGE

The evolution of sexual dichromatism in tanagers (family Thraupidae) was studied from a phylogenetic perspective using a molecular-based phylogeny. Mapping patterns of sexual dimorphism in plumage onto the phylogeny reveals that changes in female plumage occur more frequently than changes in male plumage. Possible explanations for this pattern include sexual selection acting on female plumage and natural selection for background matching. The results of this study and other recent phylogenetic and comparative studies suggest that factors affecting female plumage are important in shaping patterns of sexual dimorphism.     

Sex-specific ecomorphological variation and the evolution of sexual dimorphism in dwarf chameleons (Bradypodion spp.)

Natural selection can influence the evolution of sexual dimorphism through selection for sex-specific ecomorphological adaptations. The role of natural selection in the evolution of sexual dimorphism, however, has received much less attention than that of sexual selection. We examined the relationship between habitat structure and both male and female morphology, and sexual dimorphism in size and shape, across 21 populations of dwarf chameleon (genus Bradypodion). Morphological variation in dwarf chameleons was strongly associated with quantitative, multivariate aspects of habitat structure and, in most cases, relationships were congruent between the sexes. However, we also found consistent relationships between habitat and sexual dimorphism. These resulted from both differences in magnitude of ecomorphological relationships that were otherwise congruent between the sexes, as well as in sex-specific ecomorphological adaptations. Our study provides evidence that natural selection plays an important role in the evolution of sexual dimorphism.     

Broad‐scale variation in sexual dichromatism in songbirds is not explained by sex differences in exposure to predators during incubation

The evolution of sexual dichromatism provoked one of the greatest disagreements between Charles Darwin and Alfred Russel Wallace. According to Darwin the main driving force is sexual selection, whereby choosy females prefer showy males, leading to the evolution of conspicuous male plumage. On the other hand, Wallace suggested that dichromatism may arise because nest predation favors more cryptic females. To test the role of natural selection in the evolution of dichromatism we combined quantitative data on differences in parental share in nest attentiveness (representing the strength of natural selection on males vs females) with spectrophotometric measurements of dichromatism in 412 species of songbirds from 69 families. We expected to find stronger dichromatism in open‐nesting species with more divergent parental roles and in body parts exposed during incubation. Dichromatism was not related to the differences in parental share during incubation, but it was most pronounced in lekking species, migrants, and small species. Our results thus suggest that Wallace's hypothesis is not able to explain broad‐scale variation in the dichromatism of songbirds, but point to a role for sexual selection, mutual mate choice, and migration strategy in shaping the extraordinary variation in dichromatism exhibited by songbirds.     

“Reverse” sexual dichromatism in a Neotropical frog

Sexual dichromatism is widespread among animals, but examples of “reverse” sexual dichromatism, in which females are more brightly colored than males, are extremely rare. We discovered a unique case of reverse sexual dichromatism in the golden rocket frog (Anomaloglossus beebei), a diurnal Neotropical frog. Females are bright “golden” in color, and males are drab tan with brown pigmentation that darkens when they are calling. Here, we document this color variation with calibrated digital photography and further show that there is no evidence for sex‐specific habitat matching; both sexes live in the same well‐lit habitat on green bromeliad leaves. Our results suggest that color variation in this species is an intraspecific signal and provide an important exception to the general expectation that males are more visually conspicuous in species with conventional sex roles.     

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.     

No evidence that sexual selection is an 'engine of speciation' in birds

Abstract Sexual selection has been implicated as having a role in promoting speciation, as it should increase the rate of evolution of reproductive isolation, and there is some comparative evidence that sexual selection may be related to imbalances in clade size seen in resolved phylogenies. By employing a new comparative method we are able to investigate the role of sexual selection in explaining the patterns of species richness across birds. We used data for testes size as an index of post‐mating sexual selection, and sexual size dimorphism and sexual dichromatism as indices of pre‐mating sexual selection. These measures were obtained for 1031 species representing 467 genera. None of the variables investigated explained the patterns of species richness. As sexual selection may also increase extinction rates, the net effect on species richness in any given clade will depend on the balancing effects of sexual selection upon speciation and extinction rates. We suggest that variance across clades in this balance may have resulted in the lack of a relationship between species richness and sexual selection seen in birds.     

Sex‐related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the ‘rank advantage’ and the ‘differential susceptibility’ hypotheses, nor the ‘mate opportunity’ hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with ‘mate choice’ arguments, whereby females use condition‐dependent arrival date to assess mate quality.     

Sexual dichromatism in wing pigmentation of New World dragonflies follows Rensch's rule

Many animal taxa that display sexual size dimorphism (SSD) exhibit a positive allometric relationship in which the degree of dimorphism increases with body size. This macroevolutionary pattern is known as Rensch's rule. Although sexual selection is hypothesized to be the main mechanism causing this pattern, body size is influenced by several selective forces, including natural and sexual selection. Therefore, by focusing exclusively on SSD one cannot ascertain which of these selective forces drives Rensch's rule. If sexual selection is indeed the main mechanism underlying Rensch's rule, we predict that other sexually selected traits, including coloration‐based ornaments, will also exhibit interspecific allometric scaling consistent with Rensch's rule. We tested this prediction using wing pigmentation of 89 species of dragonflies. Studies show that male wing pigmentation is generally under strong intra‐ and intersexual selection, so that sexual dichromatism in this trait should follow Rensch's rule. Conversely, the available evidence suggests that male body size is usually not sexually selected in dragonflies, so we do not expect SSD to follow Rensch's rule. First, we found that sexual dichromatism in wing pigmentation was consistent with Rensch's rule. The phylogenetic major axis regression slope was significantly greater than one. We also showed that the allometric slope for SSD was not different from unity, providing no support for Rensch's rule. Our results provide the first evidence that a trait which appears to be under strong sexual selection exhibits a pattern consistent with Rensch's rule.     

Sexual selection is positively associated with ecological generalism among agamid lizards

Natural and sexual selection shape the evolution of species but the interplay between them is poorly understood. Two phylogenetic studies on birds have suggested that species with greater sexual dichromatism have a broader habitat use. We show that in agamid lizards, species with more elaborate secondary sexual traits are also ecologically more opportunistic. Species with greater dimorphism in head size and ornamentation have greater altitudinal range and broader habitat use, respectively, and species with greater sexual dichromatism have wider microhabitat use. Body size was positively associated with sexual and ecological generalism, but associations between ecological and sexual traits remained after accounting for body size. We suggest that sexual and natural selection may be linked either because sexual selection can promote generalism at the population level by favouring 'good genes', or because higher population densities may be associated with both stronger sexual selection and broader resource use.     

Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)

Hypotheses for the origin and maintenance of sexual size dimorphism (SSD) fall into three primary categories: (i) sexual selection on male size, (ii) fecundity selection on female size and (iii) ecological selection for gender‐specific niche divergence. We investigate the impact of these forces on SSD evolution in New World pitvipers (Crotalinae). We constructed a phylogeny from up to eight genes (seven mitochondrial, one nuclear) for 104 species of NW crotalines. We gathered morphological and ecological data for 82 species for comparative analyses. There is a strong signal of sexual selection on male size driving SSD, but less evidence for fecundity selection on female size across lineages. No support was found for allometric scaling of SSD (Rensch's rule), nor for directional selection for increasing male size (the Fairbairn–Preziosi hypothesis) in NW crotalines. Interestingly, arboreal lineages experience higher rates of SSD evolution and a pronounced shift to female‐biased dimorphism. This suggests that fecundity selection on arboreal females exaggerates ecologically mediated dimorphism, whereas sexual selection drives male size in terrestrial lineages. We find that increasing SSD in both directions (male‐ and female‐biased) decreases speciation rates. In NW crotalines, it appears that increasing magnitudes of ecologically mediated SSD reduce rates of speciation, as divergence accumulates within species among sexes, reducing adaptive divergence between populations leading to speciation.     

Antagonistic responses to natural and sexual selection and the sex-specific evolution of cuticular hydrocarbons in Drosophila simulans

Natural and sexual selection are classically thought to oppose one another, and although there is evidence for this, direct experimental demonstrations of this antagonism are largely lacking. Here, we assessed the effects of sexual and natural selection on the evolution of cuticular hydrocarbons (CHCs), a character subject to both modes of selection, in Drosophila simulans. Natural selection and sexual selection were manipulated in a fully factorial design, and after 27 generations of experimental evolution, the responses of male and female CHCs were assessed. The effects of natural and sexual selection differed greatly across the sexes. The responses of female CHCs were generally small, but CHCs evolved predominantly in the direction of natural selection. For males, profiles evolved via sexual and natural selection, as well as through the interaction between the two, with some male CHC components only evolving in the direction of natural selection when sexual selection was relaxed. These results indicate sex‐specific responses to selection, and that sexual and natural selection act antagonistically for at least some combinations of CHCs.