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The Biology of Color Forward by Technological Advances That Include Spectrophotometry, Digital Imaging, Compu RESEARCH ◥ lution and function. People working in the REVIEW SUMMARY field appreciate linkages between these parallel lines of enquiry, but outsiders need the easily navigable roadmap that we provide here. VISION ECOLOGY ADVANCES: In the past 20 years, the field of animal coloration research has been propelled The biology of color forward by technological advances that include spectrophotometry, digital imaging, compu- Innes C. Cuthill, William L. Allen, Kevin Arbuckle, Barbara Caspers, ◥ tational neuroscience, in- George Chaplin, Mark E. Hauber, Geoffrey E. Hill, Nina G. Jablonski, ON OUR WEBSITE novative laboratory and Chris D. Jiggins, Almut Kelber, Johanna Mappes, Justin Marshall, Read the full article field studies, and large- Richard Merrill, Daniel Osorio, Richard Prum, Nicholas W. Roberts, at http://dx.doi. scale comparative analy- Alexandre Roulin, Hannah M. Rowland, Thomas N. Sherratt, John Skelhorn, org/10.1126/ ses, which are allowing science.aan0221 new questions to be asked. Michael P. Speed, Martin Stevens, Mary Caswell Stoddard, Devi Stuart-Fox, .................................................. Laszlo Talas, Elizabeth Tibbetts, Tim Caro* For example, we can now pose questions about the evolution of cam- ouflage based on what a prey’smainpredator BACKGROUND: The interdisciplinary field of the underlying genetics and epigenetics, the can see, and we can start to appreciate that animal coloration is growing rapidly, spanning perception of color, how color information is gene changes underlying color production have questions about the diverse ways that animals integrated with information from other senses, occurred in parallel in unrelated species. Knowl- Downloaded from use pigments and structures to generate color, and general principles underlying color’sevo- edge of the production, perception, and evolu- tionary function of coloration is poised to make contributions to areas as diverse as medicine, security, clothing, and the military, but we need to take stock before moving forward. http://science.sciencemag.org/ OUTLOOK: Here, a group of evolutionary biologists, behavioral ecologists, psycholo- gists, optical physicists, visual physiologists, geneticists, and anthropologists review this diverse area of science, daunting to the out- sider, and set out what we believe are the key questions for the future. These are how nanoscale structures are used to manipulate light; how dynamic changes in coloration oc- cur on different time scales; the genetics of coloration (including key innovations and the on August 4, 2017 extent of parallel changes in different lineages); alternative perceptions of color by different species (including wavelengths that we can- not see, such as ultraviolet); how color, pat- tern, and motion interact; and how color works together with other modalities, especially odor. From an adaptive standpoint, color can serve several functions, and the resulting patterns frequently represent a trade-off among dif- ferent evolutionary drivers, some of which are nonvisual (e.g., photoprotection). These trade- offs can vary between individuals within the same population, and color can be altered strategically on different time scales to serve different purposes. Lastly, interspecific dif- ferences in coloration, sometimes even observ- able in the fossil record, give insights into trait evolution. The biology of color is a field that typifies modern research: curiosity-led, technology-driven, multilevel, interdisciplinary, and integrative.▪ Spectacular changes to color and morphology in a cuttlefish. Color can conceal or reveal. The list of author affiliations is available in the full article online. The giant Australian cuttlefish (Sepia apama) alters the relative size of its pigment-bearing *Corresponding author. Email: [email protected] chromatophores and warps its muscular skin to switch between camouflage mode (top) and Cite this article as I. C. Cuthill et al., Science 357,eaan0221 communication mode (bottom) in under a second. (2017). DOI: 10.1126/science.aan0221 PHOTOS: © JUSTIN MARSHALL Cuthill et al., Science 357, 470 (2017) 4 August 2017 1of1 RESEARCH ◥ Whereas structural colors occupy a huge area REVIEW of color space, pigments are limited by chemis- try (14). Furthermore, animals lack many pig- ment synthesis genes that are common in plants. VISION ECOLOGY Most famously, animals cannot manufacture carotenoids, but the genes and enzymatic path- ways involved in the modification of carotenoids The biology of color into those that are used to create a range of colors are only now under scrutiny [e.g., (15)]. Lateral Innes C. Cuthill,1 William L. Allen,2 Kevin Arbuckle,2 Barbara Caspers,3 gene transfers may be involved: Aphids, for ex- George Chaplin,4 Mark E. Hauber,5,6 Geoffrey E. Hill,7 Nina G. Jablonski,4 ample, incorporate fungal genes to produce a Chris D. Jiggins,8 Almut Kelber,9 Johanna Mappes,10 Justin Marshall,11 wider spectrum of carotenoids (16). Richard Merrill,12 Daniel Osorio,13 Richard Prum,14 Nicholas W. Roberts,1 15 16,17 18 19 Genetics of color and Alexandre Roulin, Hannah M. Rowland, * Thomas N. Sherratt, John Skelhorn, evolutionary change Michael P. Speed,20 Martin Stevens,21 Mary Caswell Stoddard,22 Devi Stuart-Fox,23 In studies of variation in animal coloration, there Laszlo Talas,1 Elizabeth Tibbetts,24 Tim Caro25† was an early emphasis on understanding the consequences of coding sequence changes, such Coloration mediates the relationship between an organism and its environment in as at the MC1R gene that regulates melanin important ways, including social signaling, antipredator defenses, parasitic exploitation, production, but advances in color genetics fo- thermoregulation, and protection from ultraviolet light, microbes, and abrasion. cus on regulatory changes that can underlie Methodological breakthroughs are accelerating knowledge of the processes underlying Downloaded from co-option of genes into novel functions. For in- both the production of animal coloration and its perception, experiments are advancing stance, a ketolase enzyme that evolved to mod- understanding of mechanism and function, and measurements of color collected ify carotenoid pigments in the retina of birds noninvasively and at a global scale are opening windows to evolutionary dynamics more paved the way for the expression of red pig- generally. Here we provide a roadmap of these advances and identify hitherto unrecognized ments in bills and plumage (17); similarly, the challenges for this multi- and interdisciplinary field. ALX3 transcription factor has come to regulate the expression of melanocyte differentiation in http://science.sciencemag.org/ he study of animal coloration has a vener- (3), we lack an appreciation of the developmen- striped rodents (18). able history. During the 19th century, early tal processes involved in cellular structure and Genes underlying color variation offer insight evolutionary biologists set out to explain pattern formation at optical scales (nanometers to into the predictability of evolution. Convergent T the diversity of colors that they observed as microns). Nonetheless, the field of soft condensed phenotypes commonly arise in parallel; the ac- products of natural selection (1). The 20th matter physics (4) holds great potential for new curate characterization of color phenotypes has century saw color phenotypes adopted as genet- insights into optical architectures. This will be revealed independent changes in similar genetic ic markers contributing to our understanding a critical foundation for future understanding mechanisms, leading to phenotypic similarity be- of development, genetics, and evolutionary the- of ordered self-assembly in colored biological tween species (19). For example, changes in pig- ory. In the past two decades, the field has again materials, from b-keratin in birds’ feathers (5)to mentationfromweaklytodeeplymelaniccanbe witnessed explosive growth. Coloration provides chiral or uniaxial chitin structures in beetles (6). controlled by parallel genetic changes in highly exceptional access to phenotypic diversity because Such knowledge can illuminate the costs, con- divergent lineages, such as in the case of the on August 4, 2017 we can quantify how color is perceived by the straints, and evolution of coloration. Kit ligand in pigmentation of sticklebacks and visual systems of diverse species, and humans are Across animals, coloration serves as a dynamic human skin; Oca2 in pigmentation of snakes, visual animals. Contemporary technologies enable form of information (Fig. 1). Colorful body parts are cavefish, and humans; and MC1R in numerous biologists to investigate nanoscale and cellular movedinbehavior,andbothpigmentsandstruc- birds and mammals (19). There has been evolu- mechanisms producing color; the sensory, neu- tural colors change at various temporal resolutions tionary bias toward repeated use of the same ral, and cognitive bases of color perception; and (7). Cephalopods are perhaps the most well-known genes perhaps because these represent mutations theadaptiveimplicationsofexternalappearances. example (8), but mobilization of pigments and with the smallest pleiotropic effects (19). Progress in each area is rapid, making animal nanostructures to change coloration is taxonomi- Convergence is also relevant to the genetic and coloration an exciting interdisciplinary field, but cally widespread. Considerable opportunities exist developmental processes that bias, constrain, or one with which it is difficult to keep pace. for dissecting
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