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Evolution of Coloration Patterns 427 ANRV356-CB24-17 ARI 3 September 2008 17:16 ANRV356-CB24-17 ARI 3 September 2008 17:16 ANNUAL Evolution of Coloration REVIEWS Further Click here for quick links to Annual Reviews content online, Patterns including: • Other articles in this volume 1 2,3 • Top cited articles Meredith E. Protas and Nipam H. Patel • Top downloaded articles 1 2 • Our comprehensive search Department of Integrative Biology, Department of Molecular and Cell Biology, and 3Howard Hughes Medical Institute, University of California, Berkeley, California 94720-3140; email: [email protected] by University of California - Berkeley on 04/27/09. For personal use only. Annu. Rev. Cell Dev. Biol. 2008. 24:425–46 Key Words First published online as a Review in Advance on pigmentation, morphological change, genetic mapping, mimicry July 1, 2008 Annu. Rev. Cell Dev. Biol. 2008.24:425-446. Downloaded from arjournals.annualreviews.org The Annual Review of Cell and Developmental Abstract Biology is online at cellbio.annualreviews.org There is an amazing amount of diversity in coloration patterns in na- This article’s doi: ture. The ease of observing this diversity and the recent application of 10.1146/annurev.cellbio.24.110707.175302 genetic and molecular techniques to model and nonmodel animals are Copyright c 2008 by Annual Reviews. allowing us to investigate the genetic basis and evolution of coloration All rights reserved in an ever-increasing variety of animals. It is now possible to ask ques- 1081-0706/08/1110-0425$20.00 tions about how many genes are responsible for any given pattern, what types of genetic changes have occurred to generate the diversity, and if the same underlying genetic changes occur repeatedly when coloration phenotypes arise through convergent evolution or parallel evolution. 425 ANRV356-CB24-17 ARI 3 September 2008 17:16 tion, and the ease of observing it, has made Contents the study of coloration patterns a popular and tractable subject for scientific inquiry. In the BACKGROUND..................... 426 past few decades, genetic, molecular, biochem- FUNCTIONS OF COLORATION. 426 ical, and cellular approaches in both model and EARLY GENETIC STUDIES nonmodel species have allowed us to under- OF COLORATION AND stand many details of the basis for color patterns STUDIES OF COLORATION during development. In addition, it is possible IN MODEL SYSTEMS ........... 431 to surmise, and sometimes experimentally vali- NATURAL COLOR VARIATION date, the selective pressures behind animal col- IN NONMODEL SPECIES....... 432 oration, allowing one to approach the question CANDIDATE GENE APPROACH: of how these patterns evolved. GENETIC ASSOCIATIONS IN WILD POPULATIONS ....... 433 CANDIDATE GENE APPROACH: FUNCTIONS OF COLORATION COMPARATIVE EXPRESSION When one is studying coloration from an evo- ANALYSIS ........................ 434 lutionary perspective, the first question that COMPLEMENTATION comes to mind is, What is the function of a CROSSES WITH MUTANTS particular pattern? In cases such as the dead- IN A MODEL SPECIES .......... 434 leaf butterfly, functional significance is fairly MAPPING APPROACH ............. 435 obvious: Appearing leaf-like may cause preda- THE GENETIC BASIS OF tors to misidentify potential prey (Figure 2). ENVIRONMENTAL EFFECTS The functional and evolutionary significance ON COLORATION .............. 438 of other examples, such as a zebra’s stripes, is MANY GENES OR FEW GENES? . 438 not as obvious. Many functions of coloration REGULATORY VERSUS have been proposed: concealment, thermoreg- CODING CHANGES? ........... 439 ulation, warning of toxicity, mimicry, sexual SAME GENES OR selection, and linkage to beneficial characteris- DIFFERENT GENES? ........... 439 tics such as immunity and salinity tolerance (re- STANDING VERSUS viewed in Roulin 2004). Finally, it is always pos- NOVEL VARIATION?............ 441 sible that a certain coloration pattern evolved by CONCLUSION ..................... 442 chance through processes such as genetic drift. Concealment is a very common function of coloration. Many animals, for example, sea by University of California - Berkeley on 04/27/09. For personal use only. dragons, when viewed in their natural habi- BACKGROUND tat, blend in almost perfectly with their sur- Annu. Rev. Cell Dev. Biol. 2008.24:425-446. Downloaded from arjournals.annualreviews.org The remarkable diversity of coloration patterns roundings (Figure 3a). This is all the more seen in animals is one of the most striking fea- striking when multiple populations of a sin- tures in the natural world. Examples include gle species living in different habitats have dis- Melanitis butterflies that resemble dried vege- tinct coloration forms that match each envi- tation, flounder and flatfish that are pigmented ronment (Figure 4). This phenomenon has on only one-half of their body and alter their been observed in many species; rock pocket appearance to match their surroundings, the mice, beach mice, deer mice, and fence lizards bold black and white stripes of zebras, bril- are just some examples within the vertebrates liantly colored tropical fish and birds, and cave- (Hoekstra 2006, Hoekstra et al. 2006, Mundy fish that lack pigment altogether (Figure 1). 2005). Rock pocket mice of the southwestern Countless examples exist of unique colors and United States and Mexico provide a particu- patterns for all types of animals. This varia- larly clear example. Most live predominantly on 426 Protas · Patel ANRV356-CB24-17 ARI 3 September 2008 17:16 a c e b d f Figure 1 Some samples of the diversity of animal coloration patterns. (a) Melanitis butterfly, whose underside resembles the dried vegetation on which it sits. (b) Flatfish that can change coloration on the upper side of its body to blend into the background. (c) A group of zebras with their striking black and white stripes. (d ) Blueface angelfish. (e) Rainbow lorikeet. ( f ) The unpigmented blind cave loach Nemacheilus troglocataractus, from Thailand (image courtesy of R. Borowsky). lightly colored rocks, and these mice have light- Another mechanism by which coloration colored fur. However, there are also some pop- patterns disguise an animal is by disruptive col- ulations of rock pocket mice that colonized dark oration, a phenomenon in which a color pattern lava flows (some of which are just a few thou- breaks up the animal’s form so that it is diffi- sand years old), and these individuals have dark cult to identify the real outline of the animal. fur (Hoekstra & Nachman 2003). It is thought A common way of disguising the boundaries of that the melanic form provides better camou- an animal is to hide the eyes by an eye mask flage in the lava flow environment, lessening the pattern and thus distort one of the most iden- by University of California - Berkeley on 04/27/09. For personal use only. chance of predation. tifiable features of a prey item. Also potentially Coloration is often a constant feature of an disruptive are black and white lines intersecting animal throughout its life. However, there are the outline of the animal, e.g., tapirs and pandas Annu. Rev. Cell Dev. Biol. 2008.24:425-446. Downloaded from arjournals.annualreviews.org cases when the animal’s coloration changes at (Caro 2005). different times and in different environments. Whereas many forms of coloration cam- This ability to change coloration is often ad- ouflage an animal, there are many examples vantageous for animals that move around on of conspicuous coloration used as a warning different-colored substrates. One classic exam- to potential predators. Black, red, orange, and ple is that of the cuttlefish (Figure 3b). Cuttle- yellow often indicate that the species is dis- fish skin changes in both color and texture as tasteful. The yellow and black ant, Cremato- the animal moves. It is thought that this change gaster inflata, produces chemicals, including 5- of color and pattern is advantageous for camou- n-alkyl resorcinols, that make them unpalatable flage as well as for signaling to other individuals to some predators, and the predators learn to (Barbato et al. 2007). avoid these ants (Ito et al. 2004). Often, multiple www.annualreviews.org • Evolution of Coloration Patterns 427 ANRV356-CB24-17 ARI 3 September 2008 17:16 Figure 2 The within-population morphological diversity of dead-leaf butterflies of the species Kallima inachus. The butterflies were all collected within a small geographic region. Although all the butterflies resemble dead leaves on their undersides, the variation on the basic leaf pattern is quite remarkable. This variation may help ensure that predators cannot cue on a specific pattern element to distinguish the butterflies from the general leaf litter. unpalatable species not only will use the same rarely attempted to eat Camponotus (Ito et al. bright colors but will closely mimic other 2004). species in pattern as well. This phenomenon, in Some animals also employ coloration to star- which multiple species share the same warning tle predators. For example, some moths, when coloration pattern, is called Mullerian¨ mimicry resting, rely primarily on cryptic coloration and is particularly well studied in butterflies but, when startled, raise their forewings to ex- by University of California - Berkeley on 04/27/09. For personal use only. and moths (Figures 5 and 6) (reviewed in pose a brightly colored area on their hindwings Parchem et al. 2007). Batesian mimicry, in con- (Figure 3c,d ). A variation of the startle re- trast, refers to instances in which a palatable sponse is to have a striking coloration pattern Annu. Rev. Cell Dev. Biol. 2008.24:425-446. Downloaded from arjournals.annualreviews.org species mimics the coloration pattern of an (false heads, eye spots, or vivid coloration of Mullerian¨ mimicry: unpalatable one and thereby evades predation tails) in a noncritical part of the animal to draw phenomenon in which an unpalatable (Figure 5). Ants of the genus Campono- the predators’ attention away from the most organism mimics the tus may utilize Batesian mimicry; Campono- vulnerable area of the body. appearance of another tus individuals overlap in territory with the Coloration also seems to play an important unpalatable one previously mentioned unpalatable C.
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