The Cellular and Developmental Biology of Wing Scales: Two Genera of Structurally-Colored Butterflies Provide Mechanisms for Evolution of Color Diversity
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Author(s): Null, Ryan W | Advisor(s): Patel, Nipam H | Abstract: The coloration of butterflies and moths, Lepidoptera, has been an important force in biological inquiry, providing among the first supporting evidence for biogeography, Darwinian evolution, and models of morphogen diffusion. In nature, color patterns have evolved that aid species’ navigation of many ecological interactions via crypsis, warning coloration, mate signaling, and the multiple forms of mimicry, which often lean heavily upon color to achieve their effect. Butterflies and moths as a whole have evolved the ability to produce all of the colors visible by humans, as well as into the UV range. As is true for most animals, the repertoire of pigments available for use in Lepidoptera is actually rather restricted – by and large limited to long-wavelength colors red, orange, and yellow, as well as, black and brown pigments. To expand into the short wavelength (violet, blue and green), Leps have repeatedly resorted to manufacturing photonically-active nanostructures. These harness physical properties of light to create the impression of color in an observer without having to manufacture a pigment. Despite knowledge of butterfly structural coloration for centuries, intense study has only taken off following the advent of the electron microscope, and despite interest, studies have been largely limited to descriptive studies and physical estimations of their function. I have undertaken efforts to understand the developmental and cellular underpinnings of structural coloration in butterflies. In the work presented here I have furthered the understanding of the field with a particular focus on how pigments modulate the diverse structural colors of 2 genera – the Morpho genus of the neotropics and the Achillides sub-genus of Papilio found throughout Oceania, East, and South Asia. In addition, I have addressed how scale ultrastructure is constructed in the developing pupa from a cell biological perspective. These studies have come hand-in-hand with the improvement of live-imaging techniques, which I argue, will be indispensable for future studies on scale development. What has emerged, is the suggestion that the Actin cytoskeleton, is essential for ultrastructural formation of scales including the modulation of nanostructure profiles. What’s more, I have shown that melanin is deployed to tune the saturation of structural color reflections and, in at least one case, to tune the hue of a multilayer-based structural color.Keywords:
Structural Coloration
Iridescence
Heliconius
Aposematism
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In diverse organisms, nanostructures that coherently scatter light create structural color, but how such structures are built remains mysterious. We investigate the evolution and genetic regulation of butterfly scale laminae, which are simple photonic nanostructures. In a lineage of buckeye butterflies artificially selected for blue wing color, we found that thickened laminae caused a color shift from brown to blue. Deletion of the optix patterning gene also altered color via lamina thickening, revealing shared regulation of pigments and lamina thickness. Finally, we show how lamina thickness variation contributes to the color diversity that distinguishes sexes and species throughout the genus Junonia. Thus, quantitatively tuning one dimension of scale architecture facilitates both the microevolution and macroevolution of a broad spectrum of hues. Because the lamina is an intrinsic component of typical butterfly scales, our findings suggest that tuning lamina thickness is an available mechanism to create structural color across the Lepidoptera.
Structural Coloration
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The evolutionary relationship between signals and animal senses has broad significance, with potential consequences for speciation, and for the efficacy and honesty of biological communication. Here we outline current understanding of the diversity of colour vision in two contrasting groups: the phylogenetically conservative birds, and the more variable butterflies. Evidence for coevolution of colour signals and vision exists in both groups, but is limited to observations of phenotypic differences between visual systems, which might be correlated with coloration. Here, to illustrate how one might interpret the evolutionary significance of such differences, we used colour vision modelling based on an avian eye to evaluate the effects of variation in three key characters: photoreceptor spectral sensitivity, oil droplet pigmentation and the proportions of different photoreceptor types. The models predict that physiologically realistic changes in any one character will have little effect, but complementary shifts in all three can substantially affect discriminability of three types of natural spectra. These observations about the adaptive landscape of colour vision may help to explain the general conservatism of photoreceptor spectral sensitivities in birds. This approach can be extended to other types of eye and spectra to inform future work on coevolution of coloration and colour vision.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.
Coevolution
Colour Vision
Variation (astronomy)
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Structural color is produced when nanostructures called schemochromes alter light reflected from a surface through different optic principles, in contrast with other types of colors that are produced when pigments selectively absorb certain wavelengths of light. Research on biogenic photonic nanostructures has focused primarily on bird feathers, butterfly wings and beetle elytra, ignoring other diverse groups such as spiders. We argue that spiders are a good model system to study the functions and evolution of colors in nature for the following reasons. First, these colors clearly function in spiders such as the tarantulas outside of sexual selection, which is likely the dominant driver of the evolution of structural colors in birds and butterflies. Second, within more than 44,000 currently known spider species, colors are used in every possible way based on the same sets of relatively simple materials. Using spiders, we can study how colors evolve to serve different functions under a variety of combinations of driving forces, and how those colors are produced within a relatively simple system. Here, we first review the different color-producing materials and mechanisms (i.e., light absorbing, reflecting and emitting) in birds, butterflies and beetles, the interactions between these different elements, and the functions of colors in different organisms. We then summarize the current state of knowledge of spider colors and compare it with that of birds and insects. We then raise questions including: 1. Could spiders use fluorescence as a mechanism to protect themselves from UV radiation, if they do not have the biosynthetic pathways to produce melanins? 2. What functions could color serve for nearly blind tarantulas? 3. Why are only multilayer nanostructures (thus far) found in spiders, while birds and butterflies use many diverse nanostructures? And, does this limit the diversity of structural colors found in spiders? Answering any of these questions in the future will bring spiders to the forefront of the study of structural colors in nature.
Structural Coloration
Iridescence
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The avian plumage color gamut is the complete range of plumage colors, as seen by birds themselves. We used a tetrahedral avian color stimulus space to estimate the avian plumage color gamut from a taxonomically diverse sample of 965 plumage patches from 111 avian species. Our sample represented all known types of plumage coloration mechanisms. The diversity of avian plumage colors occupies only a portion (26–30%, using violet-sensitive and ultraviolet-sensitive models, respectively) of the total available avian color space, which represents all colors birds can theoretically see and discriminate. For comparison, we also analyzed 2350 plant colors, including an expansive set of flowers. Bird plumages have evolved away from brown bark and green leaf backgrounds and have achieved some striking colors unattainable by flowers. Feather colors form discrete hue "continents," leaving vast regions of avian color space unoccupied. We explore several possibilities for these unoccupied hue regions. Some plumage colors may be difficult or impossible to make (constrained by physiological and physical mechanisms), whereas others may be disadvantageous or unattractive (constrained by natural and sexual selection). The plumage gamut of early lineages of living birds was probably small and dominated by melanin-based colors. Over evolutionary time, novel coloration mechanisms allowed plumages to colonize unexplored regions of color space. Pigmentary innovations evolved to broaden the gamut of possible communication signals. Furthermore, the independent origins of structural coloration in many lineages enabled evolutionary expansions into places unreachable by pigmentary mechanisms alone.
Plumage
Gamut
Hue
Iridescence
Structural Coloration
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Brilliant animal colors often are produced from light interacting with intricate nano-morphologies present in biological materials such as butterfly wing scales. Surveys across widely divergent butterfly species have identified multiple mechanisms of structural color production; however, little is known about how these colors evolved. Here, we examine how closely related species and populations of Bicyclus butterflies have evolved violet structural color from brown-pigmented ancestors with UV structural color. We used artificial selection on a laboratory model butterfly, B. anynana, to evolve violet scales from UV brown scales and compared the mechanism of violet color production with that of two other Bicyclus species, Bicyclus sambulos and Bicyclus medontias, which have evolved violet/blue scales independently via natural selection. The UV reflectance peak of B. anynana brown scales shifted to violet over six generations of artificial selection (i.e., in less than 1 y) as the result of an increase in the thickness of the lower lamina in ground scales. Similar scale structures and the same mechanism for producing violet/blue structural colors were found in the other Bicyclus species. This work shows that populations harbor large amounts of standing genetic variation that can lead to rapid evolution of scales' structural color via slight modifications to the scales' physical dimensions.
Structural Coloration
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Many species exhibit variation in the color of their scales, feathers, or fur. Various forms of natural selection, such as mimicry, crypsis, and species recognition, as well as sexual selection, can influence the evolution of color. Eastern Indigo Snakes (Drymarchon couperi), a federally threatened species, have coloration on the sides of the head and the chin that can vary from black to red or cream. Despite significant conservations efforts for this species, little is known about its biology in the field. Past researchers have proposed that the color variation on the head and chin is associated with the sex of the individual. Alternatively, color might vary among individuals because it is controlled by genes that are under natural selection or neutral evolution. We tested these alternative hypotheses by examining whether coloration of the sublabial, submaxillary, and ventral scales of this species differed by sex or among clutches. We used color spectrometry to characterize important aspects of color in two ways: by examining overall color differences across the entire color spectrum and by comparing differences within the ultraviolet, yellow, and red colorbands. We found that Eastern Indigo Snakes do not exhibit sexual dichromatism, but their coloration does vary among clutches; therefore, the pattern of sexual selection leading to sexual dichromatism observed in many squamates does not appear to play a role in the evolution and maintenance of color variation in Eastern Indigo Snakes. We suggest that future studies should focus on determining whether color variation in these snakes is determined by maternal effects or genetic components and if color is influenced by natural selection or neutral evolutionary processes. Studying species that exhibit bright colors within lineages that are not known for such coloration will contribute greatly to our understanding of the evolutionary and ecological factors that drive these differences.
Crypsis
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Camouflage
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Longwing butterflies, Heliconius sp., also called heliconians, are striking examples of diversity and mimicry in butterflies. Heliconians feature strongly colored patterns on their wings, arising from wing scales colored by pigments and/or nanostructures, which serve as an aposematic signal.Here, we investigate the coloration mechanisms among several species of Heliconius by applying scanning electron microscopy, (micro)spectrophotometry, and imaging scatterometry. We identify seven kinds of colored scales within Heliconius whose coloration is derived from pigments, nanostructures or both. In yellow-, orange- and red-colored wing patches, both cover and ground scales contain wavelength-selective absorbing pigments, 3-OH-kynurenine, xanthommatin and/or dihydroxanthommatin. In blue wing patches, the cover scales are blue either due to interference of light in the thin-film lower lamina (e.g., H. doris) or in the multilayered lamellae in the scale ridges (so-called ridge reflectors, e.g., H. sara and H. erato); the underlying ground scales are black. In the white wing patches, both cover and ground scales are blue due to their thin-film lower lamina, but because they are stacked upon each other and at the wing substrate, a faint bluish to white color results. Lastly, green wing patches (H. doris) have cover scales with blue-reflecting thin films and short-wavelength absorbing 3-OH-kynurenine, together causing a green color.The pigmentary and structural traits are discussed in relation to their phylogenetic distribution and the evolution of vision in this highly interesting clade of butterflies.
Heliconius
Aposematism
Structural Coloration
Nymphalidae
Spots
Black spot
Colored
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Structural Coloration
Cuticle (hair)
Iridescence
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In animals, iridescence is generated by the interaction of light with biological tissues that are nanostructured to produce thin films or diffraction gratings. Uniquely among animal visual signals, the study of iridescent coloration contributes to biological and physical sciences by enhancing our understanding of the evolution of communication strategies, and by providing insights into physical optics and inspiring biomimetic technologies useful to humans. Iridescent colours are found in a broad diversity of animal taxa ranging from diminutive marine copepods to terrestrial insects and birds. Iridescent coloration has received a surge of research interest of late, and studies have focused on both characterizing the nanostructures responsible for producing iridescence and identifying the behavioural functions of iridescent colours. In this paper, we begin with a brief description of colour production mechanisms in animals and provide a general overview of the taxonomic distribution of iridescent colours. We then highlight unique properties of iridescent signals and review the proposed functions of iridescent coloration, focusing, in particular, on the ways in which iridescent colours allow animals to communicate with conspecifics and avoid predators. We conclude with a brief overview of non-communicative functions of iridescence in animals. Despite the vast amount of recent work on animal iridescence, our review reveals that many proposed functions of iridescent coloration remain virtually unexplored, and this area is clearly ripe for future research.
Iridescence
Structural Coloration
Camouflage
Animal Behavior
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