Avian color vision and coloration : multidisciplinary evolutionary biology

A fundamental issue in biology is explaining the diversity of coloration found in nature. Birds provide some of the best-studied examples of the evolution and causes of color variation and some of the most arresting color displays in the natural world. They possess perhaps the most richly endowed visual system of any vertebrate, including UV-A sensitivity and tetrachromatic color vision over the 300-700-nm waveband. Birds provide model systems for the multidisciplinary study of animal coloration and color vision. Recent advances in understanding avian coloration and color vision are due to recognition that birds see colors in a different way than humans do and to the ready availability of small spectrometers. We summarize the state of the current field, recent trends, and likely future directions.

Iridescent structurally based coloration of eyespots correlates with mating success in the peacock

Gaudy plumage coloration is a widespread ornamental trait in birds and thought to be sexually selected. Although much attention has been devoted to structural coloration reflecting in UV, the signaling function of structural colors lacking UV reflectance and those that exhibit iridescence coloration are poorly documented. The train of the peacock (Pavo cristatus), a classical example of a sexually selected trait, is composed of iridescent structurally colored eyespots not reflecting in UV. Until today, the role played by the structural color of the eyespots in female mate choice has never been investigated using spectrometry. We measured eyespot coloration from a stationary angle (static coloration) and the change in coloration resulting from different angles (iridescent coloration). We assessed coloration with reflectance spectrometry, and we analyzed reflectance spectra using 2 methods. First, we extracted the reflectance spectra shape descriptors hue, brightness, and chroma. Second, we computed color and brightness contrasts signaled by eyespot feathers, taking peafowl color visual sensitivity into account. Iridescence was estimated by the maximal change for all parameters. Brightness was correlated with male mating success. The maximal change in color contrast was correlated with both the frequency of male visitation by females and male mating success. These results suggest that peahens can use both static and dynamic (i.e., iridescent) aspects of plumage structural coloration as signals to detect and choose their mates.

Coloration and colour vision in a parrot ring species

Ring species, in which reproductively isolated forms are connected by a chain of intermediate populations, provide valuable insights into the maintenance of trait variability, divergence in sympatry, and the how small changes can lead to species level differences. The parrot Platycercus elegans of eastern Australia is highly variable in plumage coloration in the wild, ranging from pale yellow to deep crimson in the chest, rump and head. It has been suggested as the only known parrot ring species worldwide, and one of less than ~25 ring species amongst all organisms. We test hypotheses for the information signalled by the colour variation, and for the maintenance of the variability.

Chromatic interaction between egg pigmentation and skin chromatophores in the nuptial coloration of female two-spotted gobies

In two-spotted gobies (Gobiusculus flavescens Fabricius 1779), females develop an orange belly as they approach sexual maturity. Bright belly coloration is preferred by males and has been suggested to act as a female ornament. This coloration is unusual in that it originates partly from pigmentation of the abdominal skin but also from strongly pigmented gonads directly visible through the skin. In addition, females have been observed to temporarily become more colourful during courtship and competition. To understand how gonad and skin pigmentation interact in this nuptial coloration, the potential for colour modification via regulation of skin chromatophores was investigated. Noradrenaline caused aggregation of chromatophore pigment and was used to experimentally reduce the contribution of skin chromatophores to the nuptial coloration. Chromatophore pigment aggregation caused bellies to become less colourful and abdominal skin biopsies to become less colourful and more transparent. There was a strong positive relationship between belly coloration and the coloration of the underlying gonads. This shows that belly coloration honestly reflects egg pigmentation, mainly because the transparency of the abdominal skin allows other fish to see the gonads directly. Interestingly, when noradrenaline caused pigment to aggregate and thereby increased the transparency of the skin, the relationship between belly and gonad coloration weakened. We conclude that female G. flavescens have a potential to use skin chromatophores to rapidly alter their nuptial coloration, thereby affecting the efficacy with which information about gonad coloration is conveyed.

Temporal variability in a multicomponent trait : nuptial coloration of female two-spotted gobies

Animals that breed more than once may face different environmental and physiological conditions at each reproductive event. Costs and benefits of sexual ornaments could therefore vary both within and between breeding seasons. Despite this, the ornaments are often assumed to be fixed, and temporal changes in ornamentation have rarely been investigated. Female two-spotted gobies (Gobiusculus flavescens) have colorful orange bellies when sexually mature and nest-holding males prefer females with more colorful bellies. This nuptial coloration is caused both by the carotenoids-rich gonads being directly visible through the skin and by the chromatophore pigmentation of the abdominal skin. Toward the end of the breeding season, males become rare and females become the more competitive sex. We show that female ornamentation of G. flavescens is a complex multicomponent trait and that the separate components, as well as their interactions, are variable. As gonads matured, they became more colorful while the abdominal skin became more transparent, causing more intense belly coloration in sexually mature females. However, coloration varied greatly also among fully mature females, suggesting that it may not only be a signal of readiness to spawn. Indeed, belly coloration predicted gonad carotenoid concentration, but there were several important seasonal differences in color expression. Females sampled toward the end of the breeding season were more colorful. This was due to seasonal increases in both gonad carotenoid concentration and skin coloration. Thus, at a time when competition over males is stronger and the terminal reproductive event approaches, females appear to invest more in signaling.

Does female nuptial coloration reflect egg carotenoids and clutch quality in the Two-Spotted Goby (Gobiusculus flavescens, Gobiidae)?

Summary

1 - Carotenoid-based ornamentation has often been suggested to signal mate quality, and species with such ornaments have frequently been used in studies of sexual selection.

2 - Female Gobiusculus flavescens (Two-Spotted Goby) develop colourful orange bellies during the breeding season. Belly coloration varies among mature females, and previous work has shown that nest-holding males prefer females with more colourful bellies. Because males invest heavily in offspring during incubation, the evolution of this preference can be explained if colourful females provide males with eggs of higher quality.

3 - We tested this hypothesis by allowing males to spawn with ‘colourful’ and ‘drab’ females and comparing parameters including egg carotenoid concentration, clutch size, hatchability and larval viability between groups. We also investigated relationships between egg carotenoid concentration and clutch quality parameters.

4 - Eggs from colourful females had significantly higher concentrations of total carotenoids than drab females, and photographically quantified belly coloration was a good predictor of egg carotenoid concentration.

5 - Colourful females produced slightly larger clutches, but female belly coloration was not related to any measure of clutch quality. In addition, there were no significant relationships between egg carotenoids and clutch quality. Females with high levels of egg carotenoids spawned slightly earlier, however, possibly because they were more ready to spawn or because of male mate choice.

6 - Our results call into question the generality of a causal link between egg carotenoids and offspring quality.

Coloration of cotton fibers with anisotropic silver nanoparticles

Anisotropic silver nanoparticles were assembled on cotton fibers to realize the coloration of cotton. The assembly of silver nanoparticles on fibers was achieved by linking of poly(diallyldimethylammonium chloride) (PDDA) at room temperature. The silver nanoparticle treated cotton showed different colors because of localized surface plasmon resonance (LSPR) property of silver nanoparticles. The coloration was completed through electrostatic interaction between the PDDA treated cotton surface and the anisotropic silver nanoparticles in the reaction system. Scanning electron microscopy (SEM) characterization demonstrated that the morphologies of silver nanoparticles remained unchanged during the coloration process, so the treated cotton inherited the LSPR optical features of silver nanoparticles. Moreover, the cotton colorated with silver nanoparticles showed reasonably good color fastness to washing, which will facilitate the practical application of this coloration process.

Investment in sensory structures, testis size, and wing coloration in males of a diurnal moth species: trade-offs or correlated growth?

For dioecious animals, reproductive success typically involves an exchange between the sexes of signals that provide information about mate location and quality. Typically, the elaborate, secondary sexual ornaments of males signal their quality, while females may signal their location and receptivity. In theory, the receptor structures that receive the latter signals may also become elaborate or enlarged in a way that ultimately functions to enhance mating success through improved mate location. The large, elaborate antennae of many male moths are one such sensory structure, and eye size may also be important in diurnal moths. Investment in these traits may be costly, resulting in trade-offs among different traits associated with mate location. For polyandrous species, such trade-offs may also include traits associated with paternity success, such as larger testes. Conversely, we would not expect this to be the case for monandrous species, where sperm competition is unlikely. We investigated these ideas by evaluating the relationship between investment in sensory structures (antennae, eye), testis, and a putative warning signal (orange hindwing patch) in field-caught males of the monandrous diurnal painted apple moth Teia anartoides (Lepidoptera: Lymantriidae) in southeastern Australia. As predicted for a monandrous species, we found no evidence that male moths with larger sensory structures had reduced investment in testis size. However, contrary to expectation, investment in sensory structures was correlated: males with relatively larger antennae also had relatively larger eyes. Intriguingly, also, the size of male orange hindwing patches was positively correlated with testis size.

An integrative framework for the appraisal of coloration in nature

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective

Poison frogs of the family Dendrobatidae contain cryptic as well as brightly colored, presumably aposematic species. The prevailing phylogenetic hypothesis assumes that the aposematic taxa form a monophyletic group while the cryptic species (Colostethus sensu lato) are basal and paraphyletic. Analysis of 86 dendrobatid sequences of a fragment of the 16S rRNA gene resulted in a much more complex scenario, with several clades that contained aposematic as well as cryptic taxa. Monophyly of the aposematic taxa was significantly rejected by SH-tests in an analysis with additional 12S and 16S rDNA fragments and reduced taxon sampling. The brightly colored Allobates femoralis and A. zaparo (Silverstone) comb. nov. (previously Epipedobates) belong in a clade with cryptic species of Colostethus. Additionally, Colostethus pratti was grouped with Epipedobates, and Colostethus bocagei with Cryptophyllobates. In several cases, the aposematic species have general distributions similar to those of their non-aposematic sister groups, indicating multiple instances of regional radiations in which some taxa independently acquired bright color. From a classificatory point of view, it is relevant that the type species of Minyobates, M. steyermarki, resulted as the sister group of the genus Dendrobates, and that species of Mannophryne and Nephelobates formed monophyletic clades, corroborating the validity of these genera. Leptodactylids of the genera Hylodes and Crossodactylus were not unambiguously identified as the sister group of the Dendrobatidae; these were monophyletic in all analyses and probably originated early in the radiation of Neotropical hyloid frogs.

A precautionary tale when describing species in a world of invaders: Morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata

The objective of this study was to investigate morphological variation in traits of systematic relevance and the phylogenetic position, ecology, and reproductive biology of the shrimp Lysmata rauli Laubenheimer and Rhyne, 2010 (Caridea: Hippolytidae), described based only on a single specimen collected in Salvador, Bahia, Brazil. We analyzed a total of 89 specimens from Camamu Bay, Bahia (n = 88) and from S3o Vicente estuary, São Paulo (n = 1). Considerable morphological variation was detected in the rostral spine series, number of segments on the carpus and merus of pereiopod 2, number of spiniform setae on the ventrolateral margin of merus and on the ventral margin of propodus of pereiopods 3-5. Importantly, L rauli can be distinguished neither using morphology, nor coloration from the Indo-Pacific L. vittata (Stimpson, 1860). Furthermore, molecular phylogenetic analyses (using the 16S mt DNA fragment) did not reveal any considerable genetic dissimilarities between L rauli and L vittata. Thus, our results clearly indicate that L rauli is not a new species but a junior synonym of L vittata. The high density observed within the structures of oyster farming indicates that the invasive L vittata lives in crowds in Brazil. The studied population was composed of males, hermaphrodites, and transitional individuals (having characteristics of males and hermaphrodites). The above information suggests that L rauli is a protandric simultaneous hermaphrodite, as it has been observed in all species of Lysmata that have been investigated. Lysmata vittata has invaded the southwestern Atlantic and is present in Bahia, Rio de Janeiro and S3o Paulo, Brazil. © The Crustacean Society, 2013. Published by Brill NV, Leiden.

Coloration of the testicular peritoneal sheath as a synapomorphy of triatomines (Hemiptera, Reduviidae)

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Infestation of guava by Anastrepha fraterculus (Diptera: Tephritidae): preferred ripening stages and influence of fruit peel coloration

The current study aimed to verify the preferred guava fruit ripening stage for egg laying by Anastrepha fraterculus (Diptera: Tephritidae) and to determine the influence of peel coloration of the fruits of 2 cultivars on infestation. The cultivars used were Paluma and Seculo XXI. The infestation level was evaluated in cages, considering 2 conditions: multiple-choice and nonchoice tests. The infestation levels of A. fraterculus differed between the green and the green-ripe stages in the multiple-choice test. In Paluma fruits with the nonchoice test, the infestation was highest during the ripe stage. There were no differences in infestation levels of A. fraterculus between the green and the green-ripe stages in Seculo XXI. In general, the green-ripe and the ripe stages were preferred for egg laying by A. fraterculus. In Paluma fruits there were significant correlations of infestation levels of A. fraterculus with luminosity (L) and chromaticity (C) in the nonchoice assay. In Seculo XXI fruits there was a significant correlation of infestation levels of A. fraterculus with color angle (h) in the nonchoice assay. No correlation was found between theses parameters in the multiple-choice test.