Joanna K. Hubbard

Vertebrate pigmentation: from underlying genes to adaptive function

Animal coloration is a powerful model for studying the genetic mechanisms that determine phenotype. Genetic crosses of laboratory mice have provided extensive information about the patterns of inheritance and pleiotropic effects of loci involved in pigmentation. Recently, the study of pigmentation genes and their functions has extended into wild populations, providing additional evidence that pigment gene function is largely conserved across disparate vertebrate taxa and can influence adaptive coloration, often in predictable ways. These new and integrative studies, along with those using a genetic approach to understand color perception, raise some important questions. Most notably, how does selection shape both phenotypic and genetic variation, and how can we use this information to further understand the phenotypic diversity generated by evolutionary processes?

An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population.

Glucocorticoid hormones (CORT) are predicted to promote adaptation to variable environments, yet little is known about the potential for CORT secretion patterns to respond to selection in free-living populations. We assessed the heritable variation underlying differences in hormonal phenotypes using a cross-foster experimental design with nestling North American barn swallows (Hirundo rustica erythrogaster). Using a bivariate animal model, we partitioned variance in baseline and stress-induced CORT concentrations into their additive genetic and rearing environment components and estimated their genetic correlation. Both baseline and stress-induced CORT were heritable with heritability of 0.152 and 0.343, respectively. We found that the variation in baseline CORT was best explained by rearing environment, whereas the variation in stress-induced CORT was contributed to by a combination of genetic and environmental factors. Further, we did not detect a genetic correlation between these two hormonal traits. Although rearing environment appears to play an important role in the secretion of both types of CORT, our results suggest that stress-induced CORT levels are underlain by greater additive genetic variance compared with baseline CORT levels. Accordingly, we infer that the glucocorticoid response to stress has a greater potential for evolutionary change in response to selection compared with baseline glucocorticoid secretion patterns.

Positive carotenoid balance correlates with greater reproductive performance in a wild bird.

Background Carotenoids can confer somatic and reproductive benefits, but most evidence is from captive animal experimentation or single time-point sampling. Another perhaps more informative means by which to assess physiological contributions to animal performance is by tracking an individuals ability to increase or sustain carotenoids or other health-related molecules over time, as these are likely to be temporally variable. Methodology/Principal Findings In a field study of North American barn swallows (Hirundo rustica erythrogaster), we analyzed within-individual changes in carotenoid concentrations by repeatedly sampling the carotenoid profiles of individuals over the course of the breeding season. Our results demonstrate that carotenoid concentrations of individuals are temporally dynamic and that season-long balance of these molecules, rather than single time-point samples, predict reproductive performance. This was true even when controlling for two important variables associated with reproductive outcomes: (1) timing of breeding and (2) sexually selected plumage coloration, which is itself positively correlated with and concomitantly changes with circulating carotenoid concentrations. Conclusions/Significance While reproduction itself is purported to impose health stress on organisms, these data suggest that free-ranging, high-quality individuals can mitigate such costs, by one or several genetic, environmental (diet), or physiological mechanisms. Moreover, the temporal variations in both health-linked physiological measures and morphological traits we uncover here merit further examination in other species, especially when goals include the estimation of signal information content or the costs of trait expression.

Quantitative genetics of plumage color: lifetime effects of early nest environment on a colorful sexual signal.

Phenotypic differences among individuals are often linked to differential survival and mating success. Quantifying the relative influence of genetic and environmental variation on phenotype allows evolutionary biologists to make predictions about the potential for a given trait to respond to selection and various aspects of environmental variation. In particular, the environment individuals experience during early development can have lasting effects on phenotype later in life. Here, we used a natural full-sib/half-sib design as well as within-individual longitudinal analyses to examine genetic and various environmental influences on plumage color. We find that variation in melanin-based plumage color – a trait known to influence mating success in adult North American barn swallows (Hirundo rustica erythrogaster) – is influenced by both genetics and aspects of the developmental environment, including variation due to the maternal phenotype and the nest environment. Within individuals, nestling color is predictive of adult color. Accordingly, these early environmental influences are relevant to the sexually selected plumage color variation in adults. Early environmental conditions appear to have important lifelong implications for individual reproductive performance through sexual signal development in barn swallows. Our results indicate that feather color variation conveys information about developmental conditions and maternal care alleles to potential mates in North American barn swallows. Melanin-based colors are used for sexual signaling in many organisms, and our study suggests that these signals may be more sensitive to environmental variation than previously thought.

Quantitative color variation within and across morphs of the polymorphic White-throated Sparrow

ABSTRACT Coloration has evolved to serve diverse functions, including communication. In species with discrete color polymorphisms, the extent to which color variation exists within morphs and communicates multiple messages often remains unclear. We employed reflectance spectrometry to study variation in coloration in the dimorphic White-throated Sparrow (Zonotrichia albicollis), which exhibits a “white” and “tan” morph in both sexes. We explored whether distinct color traits distinguish between morph and sex classes, and whether color variation exists within classes that might reflect differences in individual quality. Further, we asked whether sexual dichromatism is more pronounced in the white morph, in which males display greater promiscuity and aggression and, thus, may be under stronger sexual selection for conspicuous coloration. Distinct aspects of crown plumage coloration differentiated the two morphs versus the two sexes and multiple types of coloration were associated with a morph, suggesting both multiple and redundant messaging functions of coloration. The brightness of white coloration and yellow carotenoid-based coloration differentiated the morphs, whereas the brightness and saturation of brown to black melanin-based pigmentation differentiated the sexes within morphs. However, coloration also varied considerably within morph and sex classes, potentially reflecting differences in individual quality. Finally, more sexual dichromatism existed within white morph than within tan morph birds. White morph males and females differed in white and yellow coloration, which also differentiated the morphs, and in melanin-based coloration. By contrast, tan morph males and females differed only marginally in coloration, and only in terms of melanin-based coloration. Results suggest that crown coloration is a multifaceted signal, and that selection has acted differently on coloration in both the morphs and the sexes. Our study suggests that multifaceted coloration can play multiple and redundant messaging functions, shows that color variation in polymorphic species can communicate more than morph, and suggests that morph-specific reproductive strategies alter selection on coloration.

An experimental test of the effect of brood size on glucocorticoid responses, parental investment, and offspring phenotype

Because elevated glucocorticoid levels can impair reproduction, populations or species that engage in particularly valuable reproductive attempts may down-regulate the glucocorticoid stress response during reproduction (the brood value hypothesis). It is not clear, however, whether individuals rapidly modulate glucocorticoid responses based on shifting cues about the likelihood of reproductive success. By manipulating brood size to create broods that differed in potential value, we tested whether female barn swallows (Hirundo rustica) rapidly modulated the glucocorticoid stress response to promote investment in high-value broods, and whether nestling phenotype was influenced by treatment. Within-individual changes in female corticosterone, body mass, and measures of oxidative stress were unrelated to brood size treatment. Standard offspring provisioning rate did not differ across treatments; however, in the presence of a model predator, females raising enlarged broods maintained higher offspring feeding rates relative to control broods. Brood size did influence nestling phenotype. Nestlings from enlarged broods had lower body mass and higher baseline corticosterone than those from reduced broods. Finally, in adult females both baseline and stress-induced corticosterone were individually repeatable. Thus, while under moderately challenging environmental conditions brood size manipulations had context-dependent effects on parental investment, and influenced nestling phenotype, maternal glucocorticoid levels were not modulated based on brood value but were individually consistent features of phenotype during breeding.