ZEBRAFISH Volume 3, Number 1, 2006 © Mary Ann Liebert, Inc. Genetic Linkage and Color Polymorphism in the Southern Platyfish (Xiphophorus maculatus): A Model System for Studies of Color Pattern Evolution ALEXANDRA L. BASOLO ABSTRACT Color pattern polymorphisms are widespread in animals, and are found within populations, among populations, and among species. The southern platyfish, Xiphophorus maculatus, represents one of the most extreme examples of color pattern polymorphism. Extensive research with this model system for melanoma formation has resulted in an understanding of the underlying genetic basis of over 40 sex-linked and autosomal color patterns, includ- ing alleles that code for melanin, pterin, and carotenoid coloration. Research has also found that genes that affect sex determination, timing of sexual maturation, and coloration are genetically linked on the sex chromosomes. In many animals, color patterns often show strong sexual dimorphism, with conspicuous coloration limited to males. Although some of the color pattern alleles are sex-limited in platyfish, many are expressed by both sexes. Despite the abundance of work on this model system, little is known about the evolutionary processes responsible for this diversity of color pattern alleles. This review discusses what is known about platyfish coloration, and the roles that genetic linkage and variation in environmental conditions within and among populations might play in the evolution and maintenance of the extreme color pattern polymorphism exhibited by this platyfish. INTRODUCTION have favored the evolution of black vertical bars in males of the high-backed pygmy sword- XTENSIVE COLOR PATTERN DIVERSITY exists in tail, X. multilineatus.5 Ethe animal world, with variation both within Traits that increase an individual’s attrac- and among species. Such diversity likely has tiveness to the opposite sex may also increase adaptive significance. Coloration can be im- its conspicuousness to predators.6–8 Therefore, portant in reducing danger, with prey using whereas sexual selection is predicted to favor coloration to either warn predators or remain the evolution of more conspicuous coloration, cryptic to predators.1 Cryptic coloration can natural selection via predation should often fa- also be important to predators, reducing the vor the evolution of less conspicuous col- likelihood of their detection by potential prey. oration. Conspicuous red and orange col- Coloration is also known to play a role in both oration has been found to be attractive to mate choice and intrasexual competition.2 For females in a number of animals, including a va- example, mating preferences in one sex for riety of fishes, for example guppies, stickle- traits in the other sex appear to have favored backs, and swordtails.9–11 In the guppy, Poecilia the evolution of the colorful male sword in reticulata, females prefer males with larger or- green swordtails, Xiphophorus helleri.3,4 Intra- ange spot coloration.9 However, Endler7 found sexual competition, primarily competition that orange spots in guppies were smaller in among males for access to females, appears to populations with a high predation risk relative School of Biological Sciences, University of Nebraska—Lincoln, Lincoln, Nebraska. 65 66 BASOLO to populations with a low predation risk. Thus, the background; if there is a good match be- natural and sexual selection have opposing ef- tween an individual’s color pattern and the fects on the evolution of coloration in guppies; background color pattern, there will be a re- female mate choice favors orange or red spots duced likelihood of detection,7 especially at while predation disfavors these spots. In the greater distances. same study, the size of black, blue, iridescent, In addition to environmental effects on color and other colored spots also decreased when pattern conspicuousness, animals may modu- predation risk was increased. This suggests late the conspicuousness of color patterns us- that not only is red coloration conspicuous to ing a variety of behavioral mechanisms, such predators, but some black and iridescent color as expressing coloration on body sections that patterns are as well. In green swordtails, X. hel- can be facultatively hidden, using other indi- leri, natural and sexual selection appear to act viduals as a buffer between self and potential in opposition on the sword, a colorful male predators, and restricting activities to periods trait. While female green swordtails prefer when potential predators are least active. For long, multicolored swords,3,12 males from pop- example, some reef fishes limit their activities ulations with predatory fish have shorter during crepuscular hours (dawn and dusk) swords than males from populations in which when predation risk is relatively higher,14 and the predators are absent.8 guppies from high predation risk populations The conspicuousness of a color pattern, tend to school more than guppies from low pre- whether to a conspecific or a predator, can be dation populations.15 affected by environmental factors, such as am- Finally, the arrangement of color patterns on bient light conditions. For example, although the body can affect the conspicuousness of female sticklebacks, Gasterosteus aculeatus, pre- color patterns; reds or yellows contrasted ferred red males when the light environment against black can be particularly conspicuous.1 allowed the detection of red coloration, when For any given population, then, the optimal a filter blocked the transmission of red col- color pattern phenotypes are a balance between oration, females no longer exhibited the pref- different sources of selection, with the local bi- erence.10 In the green swordtail, X. helleri, fe- otic and abiotic environment playing an im- males prefer orange swords to green swords, portant role. The local environment, therefore, but when the light environment is experimen- should be highly predictive of the color pattern tally manipulated to reduce reflectance in the variation in a population residing there. When orange wavelengths, the preference is no environmental conditions are similar across a longer detected in prep.11 Likewise, in the species’ range, color patterns may also be sim- guppy, when wavelengths that reflect orange ilar. When environmental conditions are dis- are blocked, females no longer exhibit a pref- similar across a species’ range, color patterns erence for males with higher degrees of orange may be very different across populations. expression.13 In an aquatic environment, vari- Of the diverse types of coloration expressed ation in the spectral transmission of the water by animals, this review is primarily concerned stemming from differences in color and opac- with chromatophores found in the dermis, ity may also affect the perception of color pat- scales, integument, and eyes of fishes. Fox16 terns by individuals viewing from a distance, makes a distinction between two types of chro- as some predators might do while deciding matophores, those that contain biochromes whether to attack. (Reflective color patterns and those in which colors result from purely like blue and iridescence are expected to be de- physical properties, the schemochromes. Bio- tectable at longer distances.7) Under the same chromes are true pigments, such as carotenoids water conditions, however, the visual percep- (red, yellow, and orange), pterins (white, red, tion of the same color patterns by receivers in orange, and yellow), purines (white or silver), close proximity, like females attending to and melanins (reds, yellows, browns, and courting males, could be affected to a lesser de- blacks). Chromatophores that contain the red gree. Another environmental factor that can af- and orange carotenoids are termed ery- fect whether an organism is easily detected is throphores, and those that contain the yellow GENETIC LINKAGE AND COLOR POLYMORPHISM 67 carotenoids are termed xanthophores. Most an- Background on the southern platyfish imals do not appear to synthesize carotenoids de novo,17,18 but they can obtain carotenoid pig- The southern platyfish, X. maculatus, is a ments in their diet, including plant material, al- small, freshwater fish found in river drainages gae, and other animals. The melanin pigments of northern Central America east of the conti- are contained in chromatophores termed nental divide, ranging from the Rio Jamapa, melanophores. Melanin is a product of the ox- Veracruz, Mexico, to Belize and Guatemala (ex- idation of amino acids, such as tyrosine and cluding the Yucatan Peninsula). Coloration in tryptophan. A fourth type of biochrome, platyfish is highly variable, but the background pterinophores, contain pterins that contribute is yellowish-beige to olive-grey in coloration. to eye coloration as well as coloration of other This background coloration consists of mi- fish tissues. Pterins can be synthesized in de- cromelanophores, xanthophores, and iri- veloping pterinophores by vertebrates and dophores.20 Platyfish are found in greatest other animals.19 numbers in ponds, ditches, small lakes, and Chromatophores that do not contain true streams, but can also be found in low numbers pigment, but instead produce structural colors, in larger rivers (personal observation). The sites are called schemochromes; the color of at which platyfish occur vary in many ways, schemochromes is the result of the interaction including the presence of piscivorous fish, the of light and cell structural configuration.16 The composition of sympatric species,