Nathan I. Morehouse

A protean palette: colour materials and mixing in birds and butterflies

While typically classified as either ‘structural’ or ‘pigmentary’, bio-optical tissues of terrestrial animals are rarely homogeneous and typically contain both a structural material such as keratin or chitin and one or more pigments. These base materials interact physically and chemically to create colours. Combinations of structured base materials and embedded pigment molecules often interact optically to produce unique colours and optical properties. Therefore, to understand the mechanics and evolution of bio-optical tissues it is critical to understand their material properties, both in isolation and in combination. Here, we review the optics and evolution of coloured tissues with a focus on their base materials, using birds and butterflies as exemplar taxa owing to the strength of our current knowledge of colour production in these animals. We first review what is known of their base materials, and then discuss the consequences of these interactions from an optical perspective. Finally, we suggest directions for future research on colour optics and evolution that will be invaluable as we move towards a fuller understanding of colour in the natural world.

Pterin pigments amplify iridescent ultraviolet signal in males of the orange sulphur butterfly, Colias eurytheme.

Animal colouration is typically the product of nanostructures that reflect or scatter light and pigments that absorb it. The interplay between these colour-producing mechanisms may influence the efficacy and potential information content of colour signals, but this notion has received little empirical attention. Wing scales in the male orange sulphur butterfly (Colias eurytheme) possess ridges with lamellae that produce a brilliant iridescent ultraviolet (UV) reflectance via thin-film interference. Curiously, these same scales contain pterin pigments that strongly absorb wavelengths below 550 nm. Given that male UV reflectance functions as a sexual signal in C. eurytheme, it is paradoxical that pigments in the wing scales are highly UV absorbing. We present spectrophotometric analyses of the wings before and after pterin removal that show that pterins both depress the amplitude of UV iridescence and suppress a diffuse UV reflectance that emanates from the scales. This latter effect enhances the directionality and spectral purity of the iridescence, and increases the signals chromaticity and potential signal content. Our findings also suggest that pterins amplify the contrast between iridescent UV reflectance and scale background colour as a males wings move during flight.

Pterin pigment granules are responsible for both broadband light scattering and wavelength selective absorption in the wing scales of pierid butterflies.

A small but growing literature indicates that many animal colours are produced by combinations of structural and pigmentary mechanisms. We investigated one such complex colour phenotype: the highly chromatic wing colours of pierid butterflies including oranges, yellows and patterns which appear white to the human eye, but strongly absorb the ultraviolet (UV) wavelengths visible to butterflies. Pierids produce these bright colours using wing scales that contain collections of minute granules. However, to date, no work has directly characterized the molecular composition or optical properties of these granules. We present results that indicate these granules contain pterin pigments. We also find that pterin granules increase light reflection from single wing scales, such that wing scales containing denser granule arrays reflect more light than those with less dense granule collections. As male wing scales contain more pterin granules than those of females, the sexual dichromatism found in many pierid species can be explained by differences in wing scale pterin deposition. Additionally, the colour pattern elements produced by these pterins are known to be important during mating interactions in a number of pierid species. Therefore, we discuss the potential relevance of our results within the framework of sexual selection and colour signal evolution.

In the Eyes of the Beholders: Female Choice and Avian Predation Risk Associated with an Exaggerated Male Butterfly Color

Color ornaments are often viewed as products of countervailing sexual and natural selection, because more colorful, more attractive individuals may also be more conspicuous to predators. However, while evidence for such countervailing selection exists for vertebrate color ornaments (e.g., Trinidadian guppies), similar studies have yet to be reported in invertebrates. Indeed, evidence for female mate choice based on extant variation in male coloration is limited in invertebrates, and researchers have not explicitly asked whether more attractive males are also more conspicuous to predators. Here we provide evidence that more chromatic male cabbage white butterflies (Pieris rapae) are more attractive to females but should also be more conspicuous to predators. Female P. rapae preferentially mate with more chromatic males when choosing from populations of males with naturally occurring or commensurate, experimentally induced color variation. Mathematical models of female color vision confirm that females should be able to discriminate color differences between prospective mates. Further, chromatic and luminance contrast scores from female visual system models better predicted male mating success than did measures of male color derived more directly from color spectra. Last, models of avian color vision suggest that preferred males should be more conspicuous to known avian predators.

Quantifying iridescent coloration in animals: a method for improving repeatability

Quantification of animal colors is important to a variety of fields of research, especially those dealing with visual communication and sexual selection. Most animal colors are easily measured using well-established spectrophotometric techniques. However, the unique characteristics of iridescent colors present particular challenges and opportunities to quantify novel color metrics. Due to the fine-scale angle dependence of iridescent coloration, color metrics, such as hue and brightness, must be measured using methods that allow for repeatable comparison across individuals (e.g., by carefully controlling and measuring viewing geometry). Here, we explain how the optical characteristics of iridescent colors should be considered when developing measurement techniques, describe the pitfalls of some commonly used techniques, and recommend improved methods and metrics (angular degree of color change and breadth of reflectance) for quantifying iridescent color. In particular, most studies of iridescent birds to date have used less than ideal procedures and have not provided repeatability estimates for their methods. For example, we demonstrate here that measuring coloration from overlapping patches of iridescent feathers may be problematic, and we argue against methods that do not carefully control viewing geometry. We recommend measuring iridescence at maximal reflectance angles using an apparatus that allows for sample rotation, and we compare this technique to some other commonly used methods using iridescent gorget and crown feathers from Anna’s hummingbirds (Calypte anna). Our apparatus allows for the quantification of angular color change, and we found that maximal reflectance measurements using single feathers are highly repeatable both within feather samples and among samples within an individual.

Iridescence: views from many angles

Iridescent colours have been fascinating to humans throughout history; they are flashy, shimmering, dynamic, and examples surround us, from the commonly seen iridescent sheen of oily street puddles to the exotic, gaudy displays of birds-of-paradise featured in nature documentaries. Iridescent colours and the structures that produce them have unique properties in comparison with other types of colourants found in nature. Scientists from a variety of disciplines study the optics, development, heritability, chemical make-up, origin, evolution, functions and biomimetic technological applications of naturally occurring iridescent colours. For the first time, graduate students at Arizona State University brought together these scientists, along with educators and artists, at ‘Iridescence: more than meets the eye’, a conference to promote interdisciplinary communication and collaboration in the study of iridescent coloration from all of these perspectives. Here, we summarize the outcomes of this conference, introduce the papers that follow in this special journal issue and briefly review the current status of our understanding of iridescence.

Pesticide tolerance in amphibians: induced tolerance in susceptible populations, constitutive tolerance in tolerant populations.

The role of plasticity in shaping adaptations is important to understanding the expression of traits within individuals and the evolution of populations. With increasing human impacts on the environment, one challenge is to consider how plasticity shapes responses to anthropogenic stressors such as contaminants. To our knowledge, only one study (using mosquitoes) has considered the possibility of induced insecticide tolerance. Using populations of wood frogs (Lithobates sylvaticus) located close to and far from agricultural fields, we discovered that exposing some populations of embryos and hatchlings to sublethal concentrations of the insecticide carbaryl induced higher tolerance to a subsequent lethal concentration later in life. Interestingly, the inducible populations were located >800 m from agricultural areas and were the most susceptible to the insecticide. In contrast, the noninducible populations were located close to agricultural areas and were the least susceptible. We also found that sublethal concentrations of carbaryl induced higher tadpole AChE concentrations in several cases. This is the first study to demonstrate inducible tolerance in a vertebrate species and the pattern of inducible and constitutive tolerance among populations suggests the process of genetic assimilation.

Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly Ischnura elegans

Coexistence of female colour morphs in animal populations is often considered the result of sexual conflict, where polymorphic females benefit from reduced male sexual harassment. Mate-searching males easily detect suitable partners when only one type of female is present, but become challenged when multiple female morphs coexist, which may result in frequency-dependent mate preferences. Intriguingly, in damselflies, one female morph often closely resembles the conspecific male in body coloration, which has lead to hypotheses regarding intra-specific male-mimicry. However, few studies have quantitatively evaluated the correspondence between colour reflectance spectra from males and male-like females, relying instead on qualitative visual assessments of coloration. Using colour analyses of reflectance spectra, we compared characteristics of the body coloration of ontogenetic male and female colour morphs of the damselfly Ischnura elegans. In addition, we evaluated whether males appear to (1) discriminate between immature and mature female colour morphs, and (2) whether male-like females experience reduced male mating attention and low mating frequencies as predicted from male-mimicry. Spectral reflectance data show that immature female morphs differ substantially in coloration from mature individuals. Mating frequencies were much lower for immature than mature female morphs. For the male-like female morph, measures of colour were statistically indistinguishable from that of both immature and mature conspecific males. Mating frequencies of male-like females were lower than those of other mature female morphs under field and experimental conditions. Together, our results indicate that males may use the observed spectral differences in mate choice decisions. Furthermore, male-like females may be regarded as functional mimics that have reduced attractiveness and lowered rates of sexual harassment by mate-searching males.

Life-history evolution in the anthropocene: effects of increasing nutrients on traits and trade-offs.

Variation in life‐history traits can have major impacts on the ecological and evolutionary responses of populations to environmental change. Life‐history variation often results from trade‐offs that arise because individuals have a limited pool of resources to allocate among traits. However, human activities are increasing the availability of many once‐limited resources, such as nitrogen and phosphorus, with potentially major implications for the expression and evolution of life‐history trade‐offs. In this review, we synthesize contemporary life history and sexual selection literature with current research on ecosystem nutrient cycling to highlight novel opportunities presented by anthropogenic environmental change for investigating life‐history trait development and evolution. Specifically, we review four areas where nutrition plays a pivotal role in life‐history evolution and explore possible implications in the face of rapid, human‐induced change in nutrient availability. For example, increases in the availability of nutrients may relax historical life‐history trade‐offs and reduce the honesty of signaling systems. We argue that ecosystems experiencing anthropogenic nutrient inputs present a powerful yet underexplored arena for testing novel and longstanding questions in organismal life‐history evolution.

Digestive Organ in the Female Reproductive Tract Borrows Genes from Multiple Organ Systems to Adopt Critical Functions

Persistent adaptive challenges are often met with the evolution of novel physiological traits. Although there are specific examples of single genes providing new physiological functions, studies on the origin of complex organ functions are lacking. One such derived set of complex functions is found in the Lepidopteran bursa copulatrix, an organ within the female reproductive tract that digests nutrients from the male ejaculate or spermatophore. Here, we characterized bursa physiology and the evolutionary mechanisms by which it was equipped with digestive and absorptive functionality. By studying the transcriptome of the bursa and eight other tissues, we revealed a suite of highly expressed and secreted gene products providing the bursa with a combination of stomach-like traits for mechanical and enzymatic digestion of the male spermatophore. By subsequently placing these bursa genes in an evolutionary framework, we found that the vast majority of their novel digestive functions were co-opted by borrowing genes that continue to be expressed in nonreproductive tissues. However, a number of bursa-specific genes have also arisen, some of which represent unique gene families restricted to Lepidoptera and may provide novel bursa-specific functions. This pattern of promiscuous gene borrowing and relatively infrequent evolution of tissue-specific duplicates stands in contrast to studies of the evolution of novelty via single gene co-option. Our results suggest that the evolution of complex organ-level phenotypes may often be enabled (and subsequently constrained) by changes in tissue specificity that allow expression of existing genes in novel contexts, such as reproduction. The extent to which the selective pressures encountered in these novel roles require resolution via duplication and sub/neofunctionalization is likely to be determined by the need for specialized reproductive functionality. Thus, complex physiological phenotypes such as that found in the bursa offer important opportunities for understanding the relative role of pleiotropy and specialization in adaptive evolution.