Mechanisms Of Colour Production Research Articles

The genomics of mimicry: Gene expression throughout development provides insights into convergent and divergent phenotypes in a Müllerian mimicry system.

A common goal in evolutionary biology is to discern the mechanisms that produce the astounding diversity of morphologies seen across the tree of life. Aposematic species, those with a conspicuous phenotype coupled with some form of defence, are excellent models to understand the link between vivid colour pattern variations, the natural selection shaping it, and the underlying genetic mechanisms underpinning this variation. Mimicry systems in which species share a conspicuous phenotype can provide an even better model for understanding the mechanisms of colour production in aposematic species, especially if comimics have divergent evolutionary histories. Here we investigate the genetic mechanisms by which mimicry is produced in poison frogs. We assembled a 6.02-Gbp genome with a contig N50 of 310 Kbp, a scaffold N50 of 390 Kbp and 85% of expected tetrapod genes. We leveraged this genome to conduct gene expression analyses throughout development of four colour morphs of Ranitomeya imitator and two colour morphs from both R. fantastica and R. variabilis which R. imitator mimics. We identified a large number of pigmentation and patterning genes differentially expressed throughout development, many of them related to melanophores/melanin, iridophore development and guanine synthesis. We also identify the pteridine synthesis pathway (including genes such as qdpr and xdh) as a key driver of the variation in colour between morphs of these species, and identify several plausible candidates for colouration in vertebrates (e.g. cd36, ep-cadherin and perlwapin). Finally, we hypothesise that keratin genes (e.g. krt8) are important for producing different structural colours within these frogs.

A histological analysis of coloration in the Peruvian mimic poison frog (Ranitomeya imitator).

Aposematism continues to be a phenomenon of central interest in evolutionary biology. The life history of the mimic poison frog, Ranitomeya imitator, relies heavily on aposematism. In order for aposematic signals to be effective, predators must be able to learn to avoid the associated phenotype. However, in R. imitator, aposematism is associated with four different color phenotypes that mimic a complex of congeneric species occurring across the mimic frog's geographic range. Investigations of the underlying mechanics of color production in these frogs can provide insights into how and why these different morphs evolved. We used histological samples to examine divergence in the color production mechanisms used by R. imitator to produce effective aposematic signals across its geographic range. We measured the coverage of melanophores and xanthophores (the area covered by chromatophores divided by total area of the skin section) in each color morph. We find that morphs that produce orange skin exhibit a higher coverage of xanthophores and lower coverage of melanophores than those that produce yellow skin. In turn, morphs that produce yellow skin exhibit a higher coverage of xanthophores and lower coverage of melanophores than those that produce green skin. Generally, across the morphs, a high ratio of xanthophores to melanophores is associated with colors of brighter spectral reflectance. Together, our results contribute to the understanding of color production in amphibians and document divergence in the histology of a species that is subject to divergent selection associated with aposematism.

A combination of red structural and pigmentary coloration in the eyespot of a copepod.

While the specific mechanisms of colour production in biological systems are diverse, the mechanics of colour production are straightforward and universal. Colour is produced through the selective absorption of light by pigments, the scattering of light by nanostructures or a combination of both. When Tigriopus californicus copepods were fed a carotenoid-limited diet of yeast, their orange-red body coloration became faint, but their eyespots remained unexpectedly bright red. Raman spectroscopy indicated a clear signature of the red carotenoid pigment astaxanthin in eyespots; however, refractive index matching experiments showed that eyespot colour disappeared when placed in ethyl cinnamate, suggesting a structural origin for the red coloration. We used transmission electron microscopy to identify consecutive nanolayers of spherical air pockets that, when modelled as a single thin film layer, possess the correct periodicity to coherently scatter red light. We then performed microspectrophotometry to quantify eyespot coloration and confirmed a distinct colour difference between the eyespot and the body. The observed spectral reflectance from the eyespot matched the reflectance predicted from our models when considering the additional absorption by astaxanthin. Together, this evidence suggests the persistence of red eyespots in copepods is the result of a combination of structural and pigmentary coloration.

The genomics of mimicry: Gene expression throughout development provides insights into convergent and divergent phenotypes in a Müllerian mimicry system.

A common goal in evolutionary biology is to discern the mechanisms that produce the astounding diversity of morphologies seen across the tree of life. Aposematic species, those with a conspicuous phenotype coupled with some form of defence, are excellent models to understand the link between vivid colour pattern variations, the natural selection shaping it, and the underlying genetic mechanisms underpinning this variation. Mimicry systems in which multiple species share the same conspicuous phenotype can provide an even better model for understanding the mechanisms of colour production in aposematic species, especially if comimics have divergent evolutionary histories. Here we investigate the genetic mechanisms by which vivid colour and pattern are produced in a Müllerian mimicry complex of poison frogs. We did this by first assembling a high‐quality de novo genome assembly for the mimic poison frog Ranitomeya imitator. This assembled genome is 6.8 Gbp in size, with a contig N50 of 300 Kbp R. imitator and two colour morphs from both Ranitomeya fantastica and R. variabilis which R. imitator mimics. We identified a large number of pigmentation and patterning genes that are differentially expressed throughout development, many of them related to melanocyte development, melanin synthesis, iridophore development and guanine synthesis. Polytypic differences within species may be the result of differences in expression and/or timing of expression, whereas convergence for colour pattern between species does not appear to be due to the same changes in gene expression. In addition, we identify the pteridine synthesis pathway (including genes such as qdpr and xdh) as a key driver of the variation in colour between morphs of these species. Finally, we hypothesize that genes in the keratin family are important for producing different structural colours within these frogs.

Blue, Black, and Stripes: Evolution and Development of Color Production and Pattern Formation in Lizards and Snakes

To gain a mechanistic understanding of color pattern formation, including molecular and genetic mechanisms, it is necessary to not only describe adult phenotypes, but also to understand color production and pattern formation during embryonic and postembryonic stages. Here, we review the pigment cell mechanisms underlying color production and pattern formation during embryonic development in lizards and snakes to provide a comprehensive pigment-cell–based understanding of color pattern formation. We first focus on different color production mechanisms in terms of epidermal and dermal pigment cell architectures and then discuss the genetic determinants of pattern formation considering both biologically relevant theoretical models and the processes of pigment cell specification, migration, and architecture differentiation. Clarifying the contributions of pigment cells and genetic factors improves our general understanding of reptilian color pattern evolution.

Mechanisms for Color Convergence in a Mimetic Radiation of Poison Frogs.

In animals, bright colors often evolve to mimic other species when a resemblance is selectively favored. Understanding the proximate mechanisms underlying such color mimicry can give insights into how mimicry evolves-for example, whether color convergence evolves from a shared set of mechanisms or through the evolution of novel color production mechanisms. We studied color production mechanisms in poison frogs (Dendrobatidae), focusing on the mimicry complex of Ranitomeya imitator. Using reflectance spectrometry, skin pigment analysis, electron microscopy, and color modeling, we found that the bright colors of these frogs, both within and outside the mimicry complex, are largely structural and produced by iridophores but that color production depends crucially on interactions with pigments. Color variation and mimicry are regulated predominantly by iridophore platelet thickness and, to a lesser extent, concentration of the red pteridine pigment drosopterin. Compared with each of the four morphs of model species that it resembles, R. imitator displays greater variation in both structural and pigmentary mechanisms, which may have facilitated phenotypic divergence in this species. Analyses of nonmimetic dendrobatids in other genera demonstrate that these mechanisms are widespread within the family and that poison frogs share a complex physiological "color palette" that can produce diverse and highly reflective colors.

The golden age of arthropods: ancient mechanisms of colour production in body scales.

Insect colour is extremely diverse and produced by a large number of pigmentary and nanostructural mechanisms. Considerable research has been dedicated to these optical mechanisms, with most of it focused on chromatic colours, such as blues and greens, and less on achromatic colours like white and gold. Moreover, studies on the evolution of these colours are less common and largely limited to inferences from extant organisms, in part because of the limited amount and types of available fossil material. Here, we directly compare nanostructure and colour of extant and amber-preserved (approx. 15 and 99 Myr old, respectively) gold-coloured representatives of micromoths (Lepidoptera: Micropterigidae) and springtails (Collembola: Tomoceridae). Using electron microscopy, microspectrophotometry and finite domain time difference optical modelling, we show that golden coloration in the extant micromoth is produced by nanometre-scale crossribs that function as zero-order diffraction gratings and in the springtail by a diffraction grating without crossribs. Surprisingly, nanostructure and thus predicted colour of the amber-preserved specimens were nearly identical to those of their extant counterparts. Removal of amber enabled direct colour measurement of the fossil micromoth and further revealed that its colour matched both that of the extant specimen and the predicted colour, providing further support for our optical models. Our data thus clearly show an early origin and striking conservation of scale nanostructures and golden coloration, suggesting strong selection pressure either on the colour itself or on the mechanisms that produce the colour. Furthermore, we show the thus-far untapped potential for the use of amber-preserved specimens in studies on the evolution of organismal coloration.

Color production mechanisms in spiders

Spiders were once thought to have limited color production palettes, and even to lack melanin – one of the most ubiquitous biological pigments. Recent discoveries upend that view and show that the color production mechanisms in spiders are as elaborate as some of the more classically colorful groups of animals, such as birds, butterflies, and beetles. Here we summarize how colors are produced by spiders, identify gaps in our knowledge, show how researchers investigating color in different groups of animals can learn from each other, and suggest future opportunities for spider color research. Our understanding of color production mechanisms in other colorful groups of animals can be used as guidelines for discovering existing mechanisms previously unknown in spiders and vice versa. For example, spider species with colors potentially produced by the same kind of photonic structures previously described in white beetles, and in the blue/green scales of fishes and lizards are suggested here. In addition, novel principles first found in spiders that modify the iridescence of structural colors via the interaction of structural features across different length scales (i.e., micro-nano) may also be found in other colorful groups in the future. This review summarizes the state-of-the-art understanding regarding the proximate color production mechanisms in spiders, suggests a few future research directions that are likely to be fruitful, and facilitates the advancements in related fields, including the ecology, evolution, and functions of spider coloration.

Body coloration and mechanisms of colour production in Archelosauria: the case of deirocheline turtles.

Animal body coloration is a complex trait resulting from the interplay of multiple mechanisms. While many studies address the functions of animal coloration, the mechanisms of colour production still remain unknown in most taxa. Here we compare reflectance spectra, cellular, ultra- and nano-structure of colour-producing elements, and pigment types in two freshwater turtles with contrasting courtship behaviour, Trachemys scripta and Pseudemys concinna. The two species differ in the distribution of pigment cell-types and in pigment diversity. We found xanthophores, melanocytes, abundant iridophores and dermal collagen fibres in stripes of both species. The yellow chin and forelimb stripes of both P. concinna and T. scripta contain xanthophores and iridophores, but the post-orbital regions of the two species differ in cell-type distribution. The yellow post-orbital region of P. concinna contains both xanthophores and iridophores, while T. scripta has only xanthophores in the yellow-red postorbital/zygomatic regions. Moreover, in both species, the xanthophores colouring the yellow-red skin contain carotenoids, pterins and riboflavin, but T. scripta has a higher diversity of pigments than P. concinna. Trachemys s. elegans is sexually dichromatic. Differences in the distribution of pigment cell types across body regions in the two species may be related to visual signalling but do not match predictions based on courtship position. Our results demonstrate that archelosaurs share some colour production mechanisms with amphibians and lepidosaurs (i.e. vertical layering/stacking of different pigment cell types and interplay of carotenoids and pterins), but also employ novel mechanisms (i.e. nano-organization of dermal collagen) shared with mammals.

Red coloration varies with dietary carotenoid access and nutritional condition in kittiwakes.

Carotenoid-based ornaments are common signaling features in animals. Although the mechanisms that link color-based signals to individual condition is key to understanding the evolution and function of these ornaments, they are most often poorly known. Several hypotheses have been posited. They include: (i) the role of foraging abilities on carotenoid acquisition and thereby carotenoid-based ornaments, and (ii) the role of internal processes linked to individual quality on the allocation and conversion of carotenoids in integuments. Here, we tested the influence of dietary carotenoid access versus internal process on gape coloration in black-legged kittiwakes (Rissa tridactyla). This seabird displays a vibrant red gape, whose coloration varies with individual quality in males and is due to the deposition of red ketocarotenoids, such as astaxanthin. We decreased hydroxycarotenoid and ketocarotenoid levels in plasma, but increased efficiency in internal processes linked to nutritional condition, by supplementing breeding males with capelin, a natural energy-rich fish prey. We found that, despite having lower carotenoid levels in plasma, supplemented birds developed redder coloration than control birds, but only in the year when dietary levels of astaxanthin in the natural diet were low. In contrast, in the astaxanthin-rich year, supplemented males had a less-red gape than unsupplemented birds. These results suggest that inter-individual differences in internal processes may be sufficient to maintain the honesty of gape coloration under conditions of low dietary astaxanthin levels. Nonetheless, when inter-individual variations in dietary astaxanthin levels are elevated (such as in the crustacean-rich year), carotenoid access seems a more limiting factor to the expression of gape coloration than internal processes. Therefore, our study revealed a complex mechanism of gape color production in kittiwakes, and suggests that the main factor maintaining the condition dependency of this ornaments may vary with environmental conditions and diet composition.

Keratin nanofiber distribution and feather microstructure in penguins

ABSTRACT Penguins exhibit an array of derived feather features and color-producing mechanisms, including distinct melanosome morphologies and beta-keratin nanofibers that produce blue structural color. Several morphologies have been proposed to have hydrodynamic or insulatory functions. An understanding of the distribution of these morphologies over the body of a single penguin species may elucidate their evolution and function. We investigated feather microstructure and color production mechanisms in blue, black, and white barbs of feathers of the Gentoo Penguin (Pygoscelis papua). Light and scanning electron microscopy revealed that all feathers, regardless of color, are semi-lunate in cross section and lack, or show greatly reduced, air-filled compartments (central vacuoles) in feather barbs. Keratin nanofibers are present in all sampled feathers (including those of 8 other penguin species) but are surrounded by melanin in black barbs and disorganized in white barbs. Reduction of the air-filled central...

Spiders have rich pigmentary and structural colour palettes.

Elucidating the mechanisms of colour production in organisms is important for understanding how selection acts upon a variety of behaviours. Spiders provide many spectacular examples of colours used in courtship, predation, defence and thermoregulation, but are thought to lack many types of pigments common in other animals. Ommochromes, bilins and eumelanin have been identified in spiders, but not carotenoids or melanosomes. Here, we combined optical microscopy, refractive index matching, confocal Raman microspectroscopy and electron microscopy to investigate the basis of several types of colourful patches in spiders. We obtained four major results. First, we show that spiders use carotenoids to produce yellow, suggesting that such colours may be used for condition-dependent courtship signalling. Second, we established the Raman signature spectrum for ommochromes, facilitating the identification of ommochromes in a variety of organisms in the future. Third, we describe a potential new pigmentary-structural colour interaction that is unusual because of the use of long wavelength structural colour in combination with a slightly shorter wavelength pigment in the production of red. Finally, we present the first evidence for the presence of melanosomes in arthropods, using both scanning and transmission electron microscopy, overturning the assumption that melanosomes are a synapomorphy of vertebrates. Our research shows that spiders have a much richer colour production palette than previously thought, and this has implications for colour diversification and function in spiders and other arthropods.

Conspicuous plumage colours are highly variable.

Elaborate ornamental traits are often under directional selection for greater elaboration, which in theory should deplete underlying genetic variation. Despite this, many ornamental traits appear to remain highly variable and how this essential variation is maintained is a key question in evolutionary biology. One way to address this question is to compare differences in intraspecific variability across different types of traits to determine whether high levels of variation are associated with specific trait characteristics. Here we assess intraspecific variation in more than 100 plumage colours across 55 bird species to test whether colour variability is linked to their level of elaboration (indicated by degree of sexual dichromatism and conspicuousness) or their condition dependence (indicated by mechanism of colour production). Conspicuous colours had the highest levels of variation and conspicuousness was the strongest predictor of variability, with high explanatory power. After accounting for this, there were no significant effects of sexual dichromatism or mechanisms of colour production. Conspicuous colours may entail higher production costs or may be more sensitive to disruptions during production. Alternatively, high variability could also be related to increased perceptual difficulties inherent to discriminating highly elaborate colours. Such psychophysical effects may constrain the exaggeration of animal colours.

The effect of colour‐producing mechanisms on plumage sexual dichromatism in passerines and parrots

Summary Sexual dichromatism (SD) often reflects intense sexual selection on males. It has been hypothesized that sexual selection should favour the elaboration of those male colours that honestly signal quality and that such colours should therefore show higher SD. Costliness of colours is expected to vary according to their production mechanism (pigment type, feather microstructure and combinations thereof). Carotenoid‐based colours, due to their dietary origin and competing functions of carotenoid pigments, are the best documented costly colours, while endogenous pigments and structural colours are expected to be less costly. However, how SD varies with colour‐producing mechanism has not been systematically addressed. Here, we test the link between SD and mechanisms of colour production across nearly all Australian passerines (n = 302) and parrots (n = 48), using reflectance spectrometry and visual models. We quantified SD [chromatic (hue and saturation) and achromatic (light to dark)] for individual plumage patches as well as for the whole plumage. We then compared whether these SD estimates vary for plumage produced by different mechanisms of colour production. Not unexpectedly, individual plumage patches were most sexually dichromatic when males and females have different mechanisms of colour production. In most cases however, both sexes share the same mechanism. Among these, red carotenoid‐based plumage in passerines showed the highest SD, while in passerines as well as in parrots, melanin‐based plumage and white plumage have the lowest levels of SD. Average SD within species is weakly predicted by the proportion of the plumage produced by different mechanisms. This effect is strongest for red carotenoids, but equally so for males and females. In contrast, effects of structural and pheomelanin‐based colours are different between sexes, highlighting the links between high SD and the evolution of different mechanisms of colour production in males and females. While our analysis showed that colours based on red carotenoids have higher levels of SD, the differences were small, and most mechanisms of colour production were able to produce a similar range of SD. These results do not support the hypothesis that sexual selection should preferentially lead to the elaboration of some types of colours over others. A lay summary is available for this article.

Multiple Structural Colors of the Plumage Reflect Age, Sex, and Territory Ownership in the Eurasian MagpiePica pica

Abstract. The role of structural coloration, which is produced by the optical interactions among micro- and nanostructures in the feather barb or barbules, is still unclear in the context of sexual or social signaling, because the mechanism of color production is complex and the factors affecting it are not fully documented. We investigated whether structural colors represent class signals related to age, sex, and territory ownership in a social, sexually monochromatic species, the Eurasian Magpie Pica pica. We examined the reflectance spectra from white scapulars, bluish iridescent secondary and greenish iridescent tail plumage, as well as size of white scapular patch. Significant color differences between age classes were found in all measured plumage parts, with adults having plumage with higher color score, that is brighter, shorter wavelength-directed, and more saturated color, than young magpies. Color differences between males and females and between breeding adults (territorial owners) and non-bre...

Selection, constraint, and the evolution of coloration in African starlings.

Colorful plumage plays a prominent role in the evolution of birds, influencing communication (sexual/social selection), and crypsis (natural selection). Comparative studies have focused primarily on these selective pressures, but the mechanisms underlying color production can also be important by constraining the color gamut upon which selection acts. Iridescence is particularly interesting to study the interaction between selection and color-producing mechanisms because a broad range of colors can be produced with a shared template, and innovations to this template further expand this by increasing the parameters interacting to produce colors. We examine the patterns of ornamentation and dichromatism evolution in African starlings, a group remarkably diverse in color production mechanisms, social systems, and ecologies. We find that the presence of iridescence is ancestral to the group, being predominantly lost in females and cooperative breeders, as well as species with less labile templates. Color-producing mechanisms interact and are the main predictors of plumage ornamentation and elaboration, with little influence of selective pressures in their evolution. Dichromatism, however is influenced by social system and the loss of iridescence. Our results show the importance of considering both selection and constraints, and the different roles that they may have, in the evolution of ornamentation and dimorphism.

The colour of an avifauna: A quantitative analysis of the colour of Australian birds.

Animal coloration is a poorly-understood aspect of phenotypic variability. Here I expand initial studies of the colour gamut of birds by providing the first quantitative description of the colour variation of an entire avifauna: Australian landbirds (555 species). The colour of Australian birds occupies a small fraction (19%) of the entire possible colour space and colour variation is extremely uneven. Most colours are unsaturated, concentrated in the centre of colour space and based on the deposition of melanins. Other mechanisms of colour production are less common but account for larger portions of colour space and for most saturated colours. Male colours occupy 45–25% more colour space than female colours, indicating that sexual dichromatism translates into a broader range of male colours. Male-exclusive colours are often saturated, at the edge of chromatic space, and have most likely evolved for signalling. While most clades of birds occupy expected or lower-than-expected colour volumes, parrots and cockatoos (Order Psittaciformes) occupy a much larger volume than expected. This uneven distribution of colour variation across mechanisms of colour production, sexes and clades is probably shared by avifaunas in other parts of the world, but this remains to be tested with comparable data.

On the perception, production and function of blue colouration in animals

AbstractBright colouration in animals has long attracted the attention of physicists, chemists and biologists. As such, studies on the functions of colours are interdisciplinary, focusing on the mechanisms of colour production and maintenance, the physical and chemical properties of the colour‐producing elements, and visual systems and behaviour of potential receivers. Blue colouration has received a large share of research attention and is fascinating for several reasons: blue has been attributed to a very broad range of functions, blue is achieved by a great variety of mechanisms (although their production and maintenance costs are currently unclear), and the blue part of the spectrum (450–490 nm) can be perceived by most taxa. This review explores the breadth of studies that propose a function for blue colouration. In so doing, it discusses the diversity of ways in which blue colours are produced both as pigments and structural colours, and that blue visual pigments are common across a broad range of taxa. This analysis of the current literature emphasizes the importance of multidisciplinary hypothesis testing when attempting to elucidate the function of colours, the need for manipulative over correlative evidence for the function of colours, and, as colour research becomes evermore interdisciplinary, the need for well‐defined consistent terminology.

A Batesian mimic and its model share color production mechanisms

Abstract Batesian mimics are harmless prey species that resemble dangerous ones (models), and thus receive protection from predators. How such adaptive resemblances evolve is a classical problem in evolutionary biology. Mimicry is typically thought to be difficult to evolve, especially if the model and mimic produce the convergent phenotype through different proximate mechanisms. However, mimicry may evolve more readily if mimic and model share similar pathways for producing the convergent phenotype. In such cases, these pathways can be co-opted in ancestral mimic populations to produce high-fidelity mimicry without the need for major evolutionary innovations. Here, we show that a Batesian mimic, the scarlet kingsnake Lampropeltis elapsoides, produces its coloration using the same physiological mechanisms as does its model, the eastern coral snake Micrurus fulvius. Therefore, precise color mimicry may have been able to evolve easily in this system. Generally, we know relatively little about the proximate mechanisms underlying mimicry.

A Batesian mimic and its model share color production mechanisms

A Batesian mimic and its model share color production mechanisms