Plumage reflectance and the objective assessment of avian sexual dichromatism

Assessment of color using human vision (or standards based thereon) is central to tests of many evolutionary hypotheses. Yet fundamental differences in color Vision between humans and other animals call this approach into question. Here we use techniques for objectively assessing color patterns that avoid reliance on species-specific (e.g., human) perception. Reflectance spectra are the invariant features that we expect the animal's color cognition to have evolved to extract. We performed multivariate analyses on principal components derived from >2,600 reflectance spectra (300-720 nm) sampled in a stratified random design from different body regions of male and female starlings in breeding plumage. Starlings possess spatially complex plumage patterns and extensive areas of iridescence. Our study revealed previously unnoticed sex differences in plumage coloration and the nature of iridescent and noniridescent sex differences. Sex differences occurred in some body regions bur not others, were more pronounced at some wavelengths (both ultraviolet and human visible), and involved differences in mean reflectance and spectral shape. Discriminant analysis based on principal components were sufficient to sex correctly 100% of our sample. If hidden sexual dichromatism is widespread, then it has important implications for classifications of animals as mono- or dimorphic and for taxonomic and conservation purposes.

The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird

Ornamentation of parents poses a high risk for offspring because it reduces cryptic nest defence. Over a century ago, Wallace proposed that sexual dichromatism enhances crypsis of open-nesting females although subsequent studies found that dichromatism per se is not necessarily adaptive. We tested whether reduced female ornamentation in a sexually dichromatic species reduces the risk of clutch depredation and leads to adaptive parental roles in the red-capped plover Charadrius ruficapillus, a species with biparental incubation. Males had significantly brighter and redder head coloration than females. During daytime, when visually foraging predators are active, colour-matched model males incurred a higher risk of clutch depredation than females, whereas at night there was no difference in depredation risk between sexes. In turn, red-capped plovers maintained a strongly diurnal/nocturnal division of parental care during incubation, with males attending the nest largely at night when visual predators were inactive and females incubating during the day. We found support for Wallace's conclusion that reduced female ornamentation provides a selective advantage when reproductive success is threatened by visually foraging predators. We conclude that predators may alter their prey's parental care patterns and therefore may affect parental cooperation during care.

Flight initiation distances in relation to sexual dichromatism and body size in birds from three continents

Predators exert strong selection pressures on their prey. Prey would therefore benefit by adjusting their behaviour to the risk of predation, while predators conversely would benefit from adjusting their behaviour to that of their prey. Extravagant ornamentation has evolved to attract mates and/or successfully compete with conspecifics of the same sex to secure high mating success, even if that occurs at a cost of increased risk of predation. Thus, sexually dichromatic species may be more susceptible to predation than sexually monochromatic species, and the presence of compensation is indicative of such species being more vulnerable. If extravagant ornamentation is costly in terms of predation risk, then we should expect sexually dichromatic species to have longer flight initiation distances (FID) than sexually monochromatic species. If ornamentation is acquired as a handicap with only individuals in prime condition being able to display with the smallest viability cost, we should expect sexually dichromatic individuals to have shorter FID than sexually monochromatic individuals. Such differences among individuals should, on an evolutionary time scale, translate into differences in FID being related to differences in sexual dichromatism among species. We investigated the relationship between FID and sexual dichromatism in phylogenetic analyses, while accounting for effects of continent (Australia, North America, and Europe), body mass, the interaction between sexual dichromatism and body mass and the interaction between sexual dichromatism and continent. In an analysis of 447 species we found shorter FID in sexually dichromatic than in sexually monochromatic species (consistent with the handicap hypothesis because sexually dichromatic species took greater risks), especially so at large body size. FID differed among continents and the relative difference in FID between sexually monochromatic and sexually dichromatic species was larger in Europe than in Australia and North America. These differences among continents may be attributed to latitudinal effects of predation. These findings are important for current ideas about the evolution of secondary sexual characters because they imply covarying continental differences in predation, especially for large bodied sexually dichromatic species.

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.

Desenvolvimento do dimorfismo sexual nos macacos-de-cheiro (Saimiri VOIGT, 1831)

Os macacos-de-cheiro, Saimiri Voigt, 1831 são primatas arbóreos e ágeis, com um corpo relativamente pequeno, se comparado a outros primatas do Novo Mundo. Distribuem-se por toda a Amazônia e parte da América Central. Vários estudos foram realizados com a finalidade de estabelecer grupos taxonômicos em Saimiri. No entanto, os resultados desses estudos mostraram uma série de divergências quanto à classificação, tanto em relação à validade dos táxons, como ao status taxonômico dos mesmos. Neste gênero, observa-se a existência de diferenças sexuais no padrão de coloração da pelagem, no tamanho e forma dos dentes caninos e, ainda, um ciclo espermatogênico anual nos machos, caracterizado pela aquisição de gordura subcutânea, denominada de "condição de engorda". Durante este período, os machos apresentam um aumento de peso variando de 15 a 20%. O presente estudo teve como objetivo investigar o dimorfismo sexual em Saimiri sciureus, comparando os resultados com os de cinco outras espécies de Saimiri (S. cassiquiarensis, S. juruanus, S. ustus, S. boliviensis e S. vanzolinii). Para tanto, foram analisados 610 espécimes pertencentes às coleções do Museu Paraense Emílio Goeldi (MPEG), Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ) e Museu de Zoologia da Universidade de São Paulo (MZUSP). As classes etárias foram determinadas de acordo com a morfologia da arcada, descrita com base na seqüência eruptiva dos dentes de leite e permanentes. Foram coletados dados sobre caracteres cromáticos, onde se analisou a coloração da mancha pré-auricular de fêmeas em relação ao processo de erupção dentária, morfologia craniana para verificação de diferenciação etária e sexual, além de vinte e uma medidas cranianas, analisadas através do Teste "t" de Student. A partir dos resultados obtidos, constatou-se que não existem diferenças na coloração da pelagem entre classes sexuais anteriores à idade adulta em nenhum dos sexos. Não foram observadas diferenças na coloração da pelagem entre classes de idade em machos. A mancha pré-auricular enegrecida é um caráter exclusivo de fêmeas adultas, mas não está estritamente relacionada à ontogenia. O aparecimento do dicromatismo sexual na pelagem não é sincronizado com o aparecimento do dimorfismo na morfologia do crânio, especialmente dos dentes. Diferenças sexuais visíveis macroscopicamente, como tamanho e forma da caixa craniana, forma da face, distância bi-zigomática e forma da mandíbula podem ser evidenciadas a partir da idade subadulta. Observou-se também que o dimorfismo sexual, para todas as espécies, é melhor evidenciado em variáveis relacionadas ao aparato mastigatório. Além disso, diferenças sexuais na morfologia dos ossos do crânio podem ser claramente observadas entre os indivíduos subadultos de qualquer táxon. Os machos se tornam maiores do que as fêmeas a partir da idade subadulta, e o caráter mais conspícuo do dimorfismo sexual é o comprimento do canino. Cada espécie difere das demais por apresentar exclusividade em alguma variável (ou conjunto de variáveis) morfométricas, evidenciando dimorfismo sexual.

Sexual selection predicts brain structure in dragon lizards

Phenotypic traits such as ornaments and armaments are generally shaped by sexual selection, which often favours larger and more elaborate males compared to females. But can sexual selection also influence the brain? Previous studies in vertebrates report contradictory results with no consistent pattern between variation in brain structure and the strength of sexual selection. We hypothesize that sexual selection will act in a consistent way on two vertebrate brain regions that directly regulate sexual behaviour: the medial preoptic nucleus (MPON) and the ventromedial hypothalamic nucleus (VMN). The MPON regulates male reproductive behaviour whereas the VMN regulates female reproductive behaviour and is also involved in male aggression. To test our hypothesis, we used high-resolution magnetic resonance imaging combined with traditional histology of brains in 14 dragon lizard species of the genus Ctenophorus that vary in the strength of precopulatory sexual selection. Males belonging to species that experience greater sexual selection had a larger MPON and a smaller VMN. Conversely, females did not show any patterns of variation in these brain regions. As the volumes of both these regions also correlated with brain volume (BV) in our models, we tested whether they show the same pattern of evolution in response to changes in BV and found that the do. Therefore, we show that the primary brain nuclei underlying reproductive behaviour in vertebrates can evolve in a mosaic fashion, differently between males and females, likely in response to sexual selection, and that these same regions are simultaneously evolving in concert in relation to overall brain size.

Observations on the biology of Nothobranchius guentheri (Pfeffer) (Cyprinodontidae), an annual fish from the coastal region of East Africa

Nothobranchius guntheri is found in seasonal pools and streams in the coastal region of Tanzania. A population recurring annually in a pond near Kilosa has been studied. Growth in length was rapid and maximum mean lengths were attained within 11-12 and 7-8 weeks of hatching by males and females respectively. Males grew larger and exhibited wider variation in length than females. N. guentheri shows clear sexual dichromatism. No significant inequality in the sex ratio was found. Females with ripe eggs were found 7-8 weeks after hatching. Spawning continued throughout adult life and fecundity increased markedly with increasing length. In laboratory aquaria, aggressiveness between adult males was noted and females were actively driven on to the substratum preparatory to spawning. The diet of the fish pond consisted chiefly of aquatic and terrestrial insects, of which midge larvae and pupae were the most common. N. guentheri is exploited by man in the aquarist trade and for the biological control of mosquitoes. An extended redescription of the species is appended which includes N. melanospilus (Pfeffer) as a synonym.

Blue tits are ultraviolet tits

The blue tit (Parus caeruleus) has been classified as sexually monochromatic. This classification is based on human colour perception yet, unlike humans, most birds have four spectrally distinct classes of cone and are visually sensitive to wavelengths in the near-ultraviolet (300-400 nm). Reflectance spectrophotometry reveals that blue tit plumage shows considerable reflection of UV light. For example, the blue crest shows peak reflectance at wavelengths around 352 nm. Furthermore, the blue tit is sexually dichromatic for multiple regions of plumage, including the crest. Choice trials performed in the laboratory indicate that females prefer males with the brightest crests. This study has implications for both intra-and interspecific studies of sexual selection, as well as future classification of dichromatism, which should not ignore the possibility of variation in reflectance in the UV.

Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.

Estimating nutrient intake in comparative studies of animals: an example using dietary carotenoid content in birds

Many different methods of reporting animal diets have been used in ecological research. These vary greatly in level of accuracy and precision and therefore complicate attempts to measure and compare diets, and quantitites of nutrients in those diets, across a wide range of taxa. For most birds, the carotenoid content of the diet has not been directly measured. Here, therefore, I use an avian example to show how different methods of measuring the quantities of various foods in the diet affect the relative rankings of higher taxa (families, subfamilies, and tribes), and species within these taxa, with regard to the carotenoid contents of their diets. This is a timely example, as much recent avian literature has focused on the way dietary carotenoids may be traded off among aspects of survival, fitness and signalling. I assessed the mean dietary carotenoid contents of representatives of thirty higher taxa of birds using four different carotenoid intake indices varying in precision, including trophic levels, a coarse-scale and a fine-scale categorical index, and quantitative estimates of dietary carotenoids. This last method was used as the benchmark. For comparisons among taxa, all but the trophic level index were significantly correlated with each other. However, for comparisons of species within taxa, the fine-scale index outperformed the coarse-scale index, which in turn outperformed the trophic level index. In addition, each method has advantages and disadvantages, as well as underlying assumptions that must be considered. Examination and comparison of several possible methods of diet assessment appears to highlight these so that the best possible index is used given available data, and it is recommended that such a step be taken prior to the inclusion of estimated nutrient intake in any statistical analysis. Although applied to avian carotenoids here, this method could readily be applied to other taxa and types of nutrients.