Factors shaping the evolution of colour patterns in Australian agamid lizards (Agamidae): a comparative study

Identifying general patterns of adaptive coloration in animals can help to elucidate the evolutionary processes that generate them. We examined the evolution of colour patterns in Australian agamid lizards, a morphologically and ecologically diverse group that relies primarily on visual communication. We tested whether certain types of colour (yellow–reds and black) were likely to be used as sexual signals, as indicated by their association with indices of sexual selection, namely, sexual dichromatism and sexual dimorphism in body size and head shape. We then tested whether sexually dichromatic colours are associated with specific patterns (uniform, mottled, striped, blotched, reticulated) or ecological variables such as habitat openness, arboreality, and substrate type. The presence of yellow–red on lateral and ventral body regions and black on ventral body regions was significantly more common in males than females. Lateral yellow–red in males was associated with the total extent of sexual dichromatism and size dimorphism, whereas ventral yellow–red was associated with sexual dichromatism. Both lateral and ventral yellow–red were associated with uniform patterning, suggesting that sexual signals in male agamid lizards may often comprise uniform patches or flushes of yellow–red. Although ventral black coloration was more prevalent on males (i.e. strongly sexually dichromatic), it was not associated with indices of sexual selection, suggesting that, in agamid lizards, yellow–red coloration is more likely to be sexually selected than black. Sexually dichromatic coloration was not strongly associated with any of the ecological variables measured. We found some associations, however, between female dorsal patterns and ecological variables, suggesting that female patterns are influenced by natural selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 101–112.     

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.     

Rapid evolution of elaborate male coloration is driven by visual system in Australian fairy‐wrens (Maluridae)

The interplay between colour vision and animal signalling is of keen interest to behavioural ecologists and evolutionary biologists alike, but is difficult to address in terrestrial animals. Unlike most avian lineages, in which colour vision is relatively invariant among species, the fairy‐wrens and allies (Maluridae) show a recent gain of ultraviolet sensitivity (UVS). Here, we compare the rates of colour evolution on 11 patches for males and females across Maluridae in the context of their visual system. We measured reflectance spectra for 24 species, estimating five vision‐independent colour metrics as well as metrics of colour contrast among patches and sexual dichromatism in a receiver‐neutral colour space. We fit Brownian motion (BM) and Ornstein–Uhlenbeck (OU) models to estimate evolutionary rates for these metrics and to test whether male coloration, female coloration or dichromatism was driven by selective regimes defined by visual system or geography. We found that in general male coloration evolved rapidly in comparison with females. Male colour contrast was strongly correlated with visual system and expanded greatly in UVS lineages, whereas female coloration was weakly associated with geography (Australia vs. Papua New Guinea). These results suggest that dichromatism has evolved in Maluridae as males and females evolve at different rates, and are driven by different selection pressures.     

Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity

Sexual dichromatism, a form of sexual dimorphism in which males and females differ in colour, is widespread in animals but has been predominantly studied in birds, fishes and butterflies. Moreover, although there are several proposed evolutionary mechanisms for sexual dichromatism in vertebrates, few studies have examined this phenomenon outside the context of sexual selection. Here, we describe unexpectedly high diversity of sexual dichromatism in frogs and create a comparative framework to guide future analyses of the evolution of these sexual colour differences. We review what is known about evolution of colour dimorphism in frogs, highlight alternative mechanisms that may contribute to the evolution of sexual colour differences, and compare them to mechanisms active in other major groups of vertebrates. In frogs, sexual dichromatism can be dynamic (temporary colour change in males) or ontogenetic (permanent colour change in males or females). The degree and the duration of sexual colour differences vary greatly across lineages, and we do not detect phylogenetic signal in the distribution of this trait, therefore frogs provide an opportunity to investigate the roles of natural and sexual selection across multiple independent derivations of sexual dichromatism.     

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.     

Ecological constraint and the evolution of sexual dichromatism in darters

It is not known how environmental pressures and sexual selection interact to influence the evolution of extravagant male traits. Sexual and natural selection are often viewed as antagonistic forces shaping the evolution of visual signals, where conspicuousness is favored by sexual selection and crypsis is favored by natural selection. Although typically investigated independently, the interaction between natural and sexual selection remains poorly understood. Here, we investigate whether sexual dichromatism evolves stochastically, independent from, or in concert with habitat use in darters, a species‐rich lineage of North American freshwater fish. We find the evolution of sexual dichromatism is coupled to habitat use in darter species. Comparative analyses reveal that mid‐water darter lineages exhibit a narrow distribution of dichromatism trait space surrounding a low optimum, suggesting a constraint imposed on the evolution of dichromatism, potentially through predator‐mediated selection. Alternatively, the transition to benthic habitats coincides with greater variability in the levels of dichromatism that surround a higher optimum, likely due to relaxation of the predator‐mediated selection and heterogeneous microhabitat dependent selection regimes. These results suggest a complex interaction of sexual selection with potentially two mechanisms of natural selection, predation and sensory drive, that influence the evolution of diverse male nuptial coloration in darters.     

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.     

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.     

Dynamic sexual dichromatism in an explosively breeding Neotropical toad

Sexual selection often promotes the evolution of elaborate colour signals in males, but the importance of sexually selected colour signals remains poorly studied in amphibians. We used reflectance spectrometry to document pronounced sexual dichromatism and dramatic colour change in Bufo luetkenii, a toad that breeds in large aggregations at the onset of the rainy season in Costa Rica. Our observations suggest that males fade rapidly from a vibrant lemon yellow to a dull brown once they have paired with a female. We demonstrate this by showing that males are much brighter than females and that unpaired males are more colourful than males in amplexus. We also show that coloration fades rapidly when males are briefly held captive. This is, to our knowledge, the first study to document such dynamic change in male coloration and sexual dichromatism in anurans.     

A comparative test of adaptive hypotheses for sexual size dimorphism in lizards

It is commonly argued that sexual size dimorphism (SSD) in lizards has evolved in response to two primary, nonexclusive processes: (1) sexual selection for large male size, which confers an advantage in intrasexual mate competition (intrasexual selection hypothesis), and (2) natural selection for large female size, which confers a fecundity advantage (fecundity advantage hypothesis). However, outside of several well-studied lizard genera, the empirical support for these hypotheses has not been examined with appropriate phylogenetic control. We conducted a comparative phylogenetic analysis to test these hypotheses using literature data from 497 lizard populations representing 302 species and 18 families. As predicted by the intrasexual selection hypothesis, male aggression and territoriality are correlated with SSD, but evolutionary shifts in these categorical variables each explain less than 2% of the inferred evolutionary change in SSD. We found stronger correlations between SSD and continuous estimates of intrasexual selection such as male to female home range ratio and female home range size. These results are consistent with the criticism that categorical variables may obscure much of the actual variation in intrasexual selection intensity needed to explain patterns in SSD. In accordance with the fecundity advantage hypothesis, SSD is correlated with clutch size, reproductive frequency, and reproductive mode (but not fecundity slope, reduced major axis estimator of fecundity slope, length of reproductive season, or latitude). However, evolutionary shifts in clutch size explain less than 8% of the associated change in SSD, which also varies significantly in the absence of evolutionary shifts in reproductive frequency and mode. A multiple regression model retained territoriality and clutch size as significant predictors of SSD, but only 16% of the variation in SSD is explained using these variables. Intrasexual selection for large male size and fecundity selection for large female size have undoubtedly helped to shape patterns of SSD across lizards, but the comparative data at present provide only weak support for these hypotheses as general explanations for SSD in this group. Future work would benefit from the consideration of alternatives to these traditional evolutionary hypotheses, and the elucidation of proximate mechanisms influencing growth and SSD within populations.     

Sexual selection mediated by the thermoregulatory effects of male colour pattern in the ambush bug Phymata americana

Sexual dimorphism in coloration is a taxonomically widespread phenomenon often attributed to sexual selection on visual signals. However, the ambush bug Phymata americana exhibits sexual dimorphism in coloration that has no apparent signalling function. Here we provide evidence that colour pattern in this species influences male mating success indirectly through its effect on thermoregulation. We demonstrate, using experimental manipulation, that individuals with dark colour pattern achieve higher thoracic temperatures under illumination. We also show that dark colour pattern predicted mate-searching success but only under thermally challenging conditions (i.e. cool ambient temperature). As far as we are aware, this is the first study to provide evidence that sexual dimorphism can be accounted for by sexual selection on thermoregulatory performance.     

Habitat light sets the boundaries for the rapid evolution of cichlid fish vision,while sexual selection can tune it within those limits

Cichlid fishes' famous diversity in body coloration is accompanied by a highly diverse and complex visual system. Although cichlids possess an unusually high number of seven cone opsin genes, they express only a subset of these during their ontogeny, accounting for their astonishing interspecific variation in visual sensitivities. Much of this diversity is thought to have been shaped by natural selection as cichlids inhabit a variety of habitats with distinct light environments. Also, sexual selection might have contributed to the observed visual diversity, and sexual dimorphism in coloration potentially co‐evolved with sexual dimorphism in opsin expression. We investigated sex‐specific opsin expression of several cichlids from Africa and the Neotropics and collected and integrated data sets on sex‐specific body coloration, species‐specific visual sensitivities, lens transmission and habitat light properties for some of them. We comparatively analysed this wide range of molecular and ecological data, illustrating how integrative approaches can address specific questions on the factors and mechanisms driving diversification, and the evolution of cichlid vision in particular. We found that both sexes expressed opsins at the same levels—even in sexually dimorphic cichlid species—which argues against coevolution of sexual dichromatism and differences in sex‐specific visual sensitivity. Rather, a combination of environmental light properties and body coloration shaped the diversity in spectral sensitivities among cichlids. We conclude that although cichlids are particularly colourful and diverse and often sexually dimorphic, it would appear that natural rather than sexual selection is a more powerful force driving visual diversity in this hyperdiverse lineage.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

A mixed model of the evolution of polygyny and sexual size dimorphism in mammals

The theory of sexual selection is the most widely accepted theory explaining the evolution of mating systems and secondary sexual characters. Polygyny is the most common mating system in mammals, and there is a strong correlation between the degree of polygyny and the degree of sexual size dimorphism skewed towards males. Sexual selection theory posits that polygyny in mammals has evolved through direct, precopulatory, intrasexual selection in males, and that sexual size dimorphism is a result of male competition for mates. New results that are being obtained with the use of molecular techniques and with comparative phylogenetic methods do not appear to support predictions from this classical model in full. In this article, an expansion of the classical model is presented that combines the effects of at least four forms of selection: natural, precopulatory intrasexual, postcopulatory intrasexual, and intersexual selection. This mixed model consists of an initial phase in which natural selection operates on body size, followed by a second phase dominated by sexual selection and involving increases in sexual dimorphism and coercive behaviour of males towards females. Sexual harassment induces female aggregation, thus creating social potential for polygyny. Males compete for access to the groups of females, following two possible evolutionary scenarios, directional or equilibrium sexual selection, both producing similar behavioural polygyny, but with differences in the intensity of intra-male precopulatory sexual selection. Predictions of the mixed model are as follows: 1) polygyny can exist without high variance in male reproductive success (a fundamental requirement in the classical model); 2) extra-group fertilisation can be common; 3) sexual size dimorphism evolved prior to polygyny; 4) sexual coercion is widespread; and 5) females reduce levels of sexual coercion by joining groups.     

Ultraviolet and carotenoid‐based coloration in the viviparous lizard Zootoca vivipara (Squamata: Lacertidae) in relation to age,sex, and morphology

Lizards display structural and pigment‐based colorations, and their visual system is sensitive to wavelengths of 300–700 nm. However, few studies in squamate reptiles have quantified interindividual colour variation that includes the structural ultraviolet (UV) component (300–400 nm). In the present study, we investigated variability of a ventral UV/yellow–red ornamentation in the common lizard Zootoca vivipara, including an analysis of spatial distribution, as well as sex and age differences. We also investigated whether the expression of coloration is related to body size and condition. Our analyses revealed two distinct patches: a gular patch with a strong UV reflectance and a belly patch with a dominant yellow–red reflectance. Males displayed a less saturated throat coloration with higher UV chroma and UV hue, and had a redder but duller belly coloration than females. Yearlings had less elaborate ornaments than adults, although they already displayed a yellow–red sexual dichromatism on the belly. UV sexual dichromatism was only apparent in adults as a result of a weaker UV reflectance in females, suggesting potential fitness costs of a bright UV coloration in that sex. Different colour traits were related to body size in both sexes, as well as to body condition in males. We discuss the potential evolutionary scenarios leading to the maintenance of this ornament in common lizards. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 128–141.     

Mimetic butterflies support Wallace's model of sexual dimorphism

Theoretical and empirical observations generally support Darwin's view that sexual dimorphism evolves due to sexual selection on, and deviation in, exaggerated male traits. Wallace presented a radical alternative, which is largely untested, that sexual dimorphism results from naturally selected deviation in protective female coloration. This leads to the prediction that deviation in female rather than male phenotype causes sexual dimorphism. Here I test Wallace's model of sexual dimorphism by tracing the evolutionary history of Batesian mimicry-an example of naturally selected protective coloration-on a molecular phylogeny of Papilio butterflies. I show that sexual dimorphism in Papilio is significantly correlated with both female-limited Batesian mimicry, where females are mimetic and males are non-mimetic, and with the deviation of female wing colour patterns from the ancestral patterns conserved in males. Thus, Wallace's model largely explains sexual dimorphism in Papilio. This finding, along with indirect support from recent studies on birds and lizards, suggests that Wallace's model may be more widely useful in explaining sexual dimorphism. These results also highlight the contribution of naturally selected female traits in driving phenotypic divergence between species, instead of merely facilitating the divergence in male sexual traits as described by Darwin's model.     

The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae)

Sexual size dimorphism (SSD) evolves because body size is usually related to reproductive success through different pathways in females and males. Female body size is strongly correlated with fecundity, while in males, body size is correlated with mating success. In many lizard species, males are larger than females, whereas in others, females are the larger sex, suggesting that selection on fecundity has been stronger than sexual selection on males. As placental development or egg retention requires more space within the abdominal cavity, it has been suggested that females of viviparous lizards have larger abdomens or body size than their oviparous relatives. Thus, it would be expected that females of viviparous species attain larger sizes than their oviparous relatives, generating more biased patterns of SSD. We test these predictions using lizards of the genus Sceloporus. After controlling for phylogenetic effects, our results confirm a strong relationship between female body size and fecundity, suggesting that selection for higher fecundity has had a main role in the evolution of female body size. However, oviparous and viviparous females exhibit similar sizes and allometric relationships. Even though there is a strong effect of body size on female fecundity, once phylogenetic effects are considered, we find that the slope of male on female body size is significantly larger than one, providing evidence of greater evolutionary divergence of male body size. These results suggest that the relative impact of sexual selection acting on males has been stronger than fecundity selection acting on females within Sceloporus lizards.     

Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration

In birds, carotenoid-based plumage coloration is more dependent on physical condition and foraging abilities and less constrained developmentally than is melanin-based coloration. Thus, female mate choice for honest signals should result in more intense sexual selection on carotenoid- than on melanin-based plumage coloration. Using variation in sexual dimorphism as an indirect measure of the intensity of sexual selection, we tested the prediction mat variation in sexual dimorphism is driven more by change in carotenoid-based coloration between males and females dian by change in melanin-based coloration. Examination of historical changes in carotenoid- versus melanin-based pigmentation in 126 extant species of Cardueline finches supported this prediction. We found that carotenoid-derived coloration changed more frequendy among congeners dian melanin-based coloration. In both sexes, increase in carotenoid-based coloration score, but not in melanin-based coloration score, was strongly associated with increase in sexual dichromatism. In addition, sexual dimorphism in carotenoid-based coloration contributed more to overall dichromatism than dimorphism in melanin-based plumage. Our results supported die hypothesis that melanin-based and carotenoid-based coloration have fundamentally different signal content and suggest that combining melanin-based and carotenoid-based coloration in comparative analyses is not appropriate.     

Intrasexual selection predicts the evolution of signal complexity in lizards

Sexual selection has often been invoked in explaining extravagant morphological and behavioural adaptations that function to increase mating success. Much is known about the effects of intersexual selection, which operates through female mate choice, in shaping animal signals. The role of intrasexual selection has been less clear. We report on the first evidence for the coevolution of signal complexity and sexual size dimorphism (SSD), which is characteristically produced by high levels of male male competition. We used two complementary comparative methods in order to reveal that the use of complex signals is associated with SSD in extant species and that historical increases in complexity have occurred in regions of a phylogenetic tree characterized by high levels of pre-existing size dimorphism. We suggest that signal complexity has evolved in order to improve opponent assessment under conditions of high male male competition. Our findings suggest that intrasexual selection may play an important and previously underestimated role in the evolution of communicative systems.     

SEXUAL SELECTION AND THE EVOLUTION OF COMPLEX COLOR PATTERNS IN DRAGON LIZARDS

Many species have elaborate and complex coloration and patterning, which often differ between the sexes. Sexual selection may increase the size or intensity of color patches (elaboration) in one sex or drive the evolution of novel signal elements (innovation). The latter potentially increases color pattern complexity. Color pattern complexity may also be influenced by ecological factors related to predation and environment; however, very few studies have investigated the effects of both sexual and natural selection on color pattern complexity across species. We used a phylogenetic comparative approach to examine these effects in 85 species and subspecies of Australian dragon lizards (family Agamidae). We quantified color pattern complexity by adapting the Shannon–Wiener diversity index. There were clear sex differences in color pattern complexity, which were positively correlated with both sexual dichromatism and sexual size dimorphism, consistent with the idea that sexual selection plays a significant role in the evolution of color pattern complexity. By contrast, we found little evidence of a link between environmental factors and color pattern complexity on body regions exposed to predators. Our results suggest that sexual selection rather than natural selection has led to increased color pattern complexity in males.