Rafael Maia

pavo: an R package for the analysis, visualization and organization of spectral data

Summary Recent technical and methodological advances have led to a dramatic increase in the use of spectrometry to quantify reflectance properties of biological materials, as well as models to determine how these colours are perceived by animals, providing important insights into ecological and evolutionary aspects of animal visual communication. Despite this growing interest, a unified cross-platform framework for analysing and visualizing spectral data has not been available. We introduce pavo, an R package that facilitates the organization, visualization and analysis of spectral data in a cohesive framework. pavo is highly flexible, allowing users to (a) organize and manipulate data from a variety of sources, (b) visualize data using Rs state-of-the-art graphics capabilities and (c) analyse data using spectral curve shape properties and visual system modelling for a broad range of taxa. In this paper, we present a summary of the functions implemented in pavo and how they integrate in a workflow to explore and analyse spectral data. We also present an exact solution for the calculation of colour volume overlap in colourspace, thus expanding previously published methodologies. As an example of pavos capabilities, we compare the colour patterns of three African glossy starling species, two of which have diverged very recently. We demonstrate how both colour vision models and direct spectral measurement analysis can be used to describe colour attributes and differences between these species. Different approaches to visual models and several plotting capabilities exemplify the packages versatility and streamlined workflow. pavo provides a cohesive environment for handling spectral data and addressing complex sensory ecology questions, while integrating with Rs modular core for a broader and comprehensive analytical framework, automated management of spectral data and reproducible workflows for colour analysis.

Key ornamental innovations facilitate diversification in an avian radiation

Patterns of biodiversity are often explained by ecological processes, where traits that promote novel ways of interacting with the environment (key innovations) play a fundamental role in promoting diversification. However, sexual selection and social competition can also promote diversification through rapid evolution of ornamental traits. Because selection can operate only on existing variation, the tendency of ornamental traits to constrain or enable the production of novel phenotypes is a crucial but often overlooked aspect of diversification. Starlings are a speciose group characterized by diverse iridescent colors produced by nanometer-scale arrays of melanin-containing organelles (melanosomes) that play a central role in sexual selection and social competition. We show that evolutionary lability of these colors is associated with both morphological and lineage diversification in African starlings. The solid rod-like melanosome morphology has evolved in a directional manner into three more optically complex forms that can produce a broader range of colors than the ancestral form, resulting in (i) faster color evolution, (ii) the occupation of novel, previously unreachable regions of colorspace, and ultimately (iii) accelerated lineage diversification. As in adaptive radiations, key innovations in ornament production can provide high phenotypic trait variability, leading to dramatic effects on the tempo and mode of diversification.

Nanostructural self-assembly of iridescent feather barbules through depletion attraction of melanosomes during keratinization

Avian plumage colours are model traits in understanding the evolution of sexually selected ornamental traits. Paradoxically, iridescent structural colours, probably the most dazzling of these traits, remain the most poorly understood. Though some data suggest that expression of bright iridescent plumage colours produced by highly ordered arrays of melanosomes and keratin is condition-dependent, almost nothing is known of their ontogeny and thus of any developmental mechanisms that may be susceptible to perturbation. Here, we use light and electron microscopy to compare the ontogeny of iridescent male and non-iridescent female feathers in blue-black grassquits. Feather barbules of males contain a single layer of melanosomes bounded by a thin layer of keratin-producing blue iridescent colour, while those of females contain disorganized melanosomes and no outer layer. We found that nanostructural organization of male barbules occurs late in development, following death of the barbule cell, and is thus unlikely to be under direct cellular control, contrary to previous suggestions. Rather, organization appears to be caused by entropically driven self-assembly through depletion attraction forces that pin melanosomes to the edge of barbule cells and to one another. These forces are probably stronger in developing barbules of males than of females because their melanosomes are (i) larger, (ii) more densely packed, and (iii) more homogeneously distributed owing to the more consistent shape of barbules during keratinization. These data provide the first proposed developmental pathway for iridescent plumage colours, and suggest that any condition dependence of iridescent barbules is likely driven by factors other than direct metabolic cost.

What makes a feather shine? A nanostructural basis for glossy black colours in feathers.

Colours in feathers are produced by pigments or by nanostructurally organized tissues that interact with light. One of the simplest nanostructures is a single layer of keratin overlying a linearly organized layer of melanosomes that create iridescent colours of feather barbules through thin-film interference. Recently, it has been hypothesized that glossy (i.e. high specular reflectance) black feathers may be evolutionarily intermediate between matte black and iridescent feathers, and thus have a smooth keratin layer that produces gloss, but not the layered organization of melanosomes needed for iridescence. However, the morphological bases of glossiness remain unknown. Here, we use a theoretical approach to generate predictions about morphological differences between matte and glossy feathers that we then empirically test. Thin-film models predicted that glossy spectra would result from a keratin layer 110–180 nm thick and a melanin layer greater than 115 nm thick. Transmission electron microscopy data show that nanostructure of glossy barbules falls well within that range, but that of matte barbules does not. Further, glossy barbules had a thinner and more regular keratin cortex, as well as a more continuous underlying melanin layer, than matte barbules. Thus, their quasi-ordered nanostructures are morphologically intermediate between matte black and iridescent feathers, and perceived gloss may be a form of weakly chromatic iridescence.

The adaptive value of primate color vision for predator detection

The complex evolution of primate color vision has puzzled biologists for decades. Primates are the only eutherian mammals that evolved an enhanced capacity for discriminating colors in the green–red part of the spectrum (trichromatism). However, while Old World primates present three types of cone pigments and are routinely trichromatic, most New World primates exhibit a color vision polymorphism, characterized by the occurrence of trichromatic and dichromatic females and obligatory dichromatic males. Even though this has stimulated a prolific line of inquiry, the selective forces and relative benefits influencing color vision evolution in primates are still under debate, with current explanations focusing almost exclusively at the advantages in finding food and detecting socio‐sexual signals. Here, we evaluate a previously untested possibility, the adaptive value of primate color vision for predator detection. By combining color vision modeling data on New World and Old World primates, as well as behavioral information from human subjects, we demonstrate that primates exhibiting better color discrimination (trichromats) excel those displaying poorer color visions (dichromats) at detecting carnivoran predators against the green foliage background. The distribution of color vision found in extant anthropoid primates agrees with our results, and may be explained by the advantages of trichromats and dichromats in detecting predators and insects, respectively. Am. J. Primatol. 76:721–729, 2014.

Here comes the sun: multimodal displays are associated with sunlight incidence

Conspicuousness of courtship signals in animals likely evolved to maximize mate attraction while minimizing predator detection. It is assumed, though largely unknown, that environmental and luminosity conditions affect the detectability of ornaments and motor displays and could thus strongly influence behavior. We combined visual models and behavioral observations to test whether the multimodal display of the blue-black grassquit (Volatinia jacarina) is influenced by environmental conditions, predicting that males should display more often in moments with high sunlight incidence upon their bodies. By displaying in such a context-dependent fashion, males would be able to maximize conspicuousness of their iridescent blue-black plumage and avoid displaying continuously, since the latter would involve higher energetic investment. We recorded the rates of both complete displays (leap with singing) as well as incomplete ones (singing while perched) for males during repeated 30-min focal observations in varying environmental situations in the field. We found that when bathed directly in sunlight, males increased their rates of displays, tending to exhibit more complete rather than incomplete displays in this condition and suggesting a potential trade-off between display types. Our results suggest that animals may adjust the timing and precise location of signal activity to improve the efficiency or likelihood of detection of some signal elements.

Social environment affects testosterone level in captive male blue-black grassquits.

The challenge hypothesis proposes that testosterone (T) elevation above what is needed for breeding is associated with social factors, and males possibly modulate their hormonal response to variations in population density and sex ratio. We investigated the role of social environment in altering testosterone levels and aggression in a tropical, seasonally breeding grassquit (Volatinia jacarina). We exposed males to three social conditions during 1 year: all-males treatment (six males), mixed treatment (three males-three females), and paired treatment (one male-one female). We quantified aggressiveness among males and T plasma concentration for each individual in each treatment monthly. We found that more aggressive interactions occurred in the all-males treatment than in the mixed treatment. The data also revealed that, coincident with these behavioral changes, the patterns of T variation through time in each treatment were markedly different. The all-males treatment exhibited an early increase in T concentration, which was sustained for a lengthy period with two distinctive peaks, and subsequently declined sharply. The mixed treatment presented an intermediate pattern, with more gradual increase and decrease in T levels. At the other extreme, the paired treatment presented a later rise in T concentration. We conclude that the more competitive environment, with higher density of males, caused the early and higher elevation in T level, thus the presence of competitors may influence the decision of how much a male should invest in reproduction. We suggest that the males perception of his social environment ultimately mediates hormonal production and alters his reproductive strategy.

Iridescent colour production in hairs of blind golden moles (Chrysochloridae)

Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.

Achieving luster: prenuptial molt pattern predicts iridescent structural coloration in Blue-black Grassquits

Colors in feathers are produced by pigment deposition or by nanostructures within barbs or barbules. In the absence of pigments or nanostructures, light is scattered incoherently, producing white coloration. Honest advertisement models predict that ornamental colors evolve if they reliably signal individual properties such as viability, health, or nutritional state. In this study, we tested if (1) iridescent structural and (2) unpigmented plumage coloration signal male quality in the Blue-black Grassquit (Volatinia jacarina). During three reproductive seasons, we captured males and measured morphological variables and nuptial plumage coverage, and collected feathers for spectrometry. We found that saturation of the iridescent coloration was positively related to relative molting speed, indicating that males investing more in prenuptial molt also produced more saturated, UV-shifted plumage. Body condition was not related to brightness or saturation of the iridescent plumage, and no male morphological attributes were associated with the white underwing patch coloration or size. Our results suggest that patterns of molt, and possibly feather growth, may affect the organization of optical nanostructures responsible for iridescent coloration, and that the ontogeny of iridescent plumage ornaments must be taken into account in hypotheses concerning honest advertisement of such signals. Thus, coloration in this species may reliably reflect energy allocation to molting, constituting an honest indicator of male quality, life history decisions, or endocrine state. To our knowledge, this is the first report of natural variation in molting pattern being associated with sexually-selected structural color plumage.

The Evolution of Energetic Scaling across the Vertebrate Tree of Life

Metabolism is the link between ecology and physiology—it dictates the flow of energy through individuals and across trophic levels. Much of the predictive power of metabolic theories of ecology derives from the scaling relationship between organismal size and metabolic rate. There is growing evidence that this scaling relationship is not universal, but we have little knowledge of how it has evolved over macroevolutionary time. Here we develop a novel phylogenetic comparative method to investigate how often and in which clades the macroevolutionary dynamics of the metabolic scaling have changed. We find strong evidence that the metabolic scaling relationship has shifted multiple times across the vertebrate phylogeny. However, shifts are rare and otherwise strongly constrained. Importantly, both the estimated slope and intercept values vary widely across regimes, with slopes that spanned across theoretically predicted values such as 2/3 or 3/4. We further tested whether traits such as ecto-/endothermy, genome size, and quadratic curvature with body mass (i.e., energetic constraints at extreme body sizes) could explain the observed pattern of shifts. Though these factors help explain some of the variation in scaling parameters, much of the remaining variation remains elusive. Our results lay the groundwork for further exploration of the evolutionary and ecological drivers of major transitions in metabolic strategy and for harnessing this information to improve macroecological predictions.