Academic journal article Genetics

Pigment Pattern Formation in the Guppy, Poecilia Reticulata, Involves the Kita and Csf1ra Receptor Tyrosine Kinases

Academic journal article Genetics

Pigment Pattern Formation in the Guppy, Poecilia Reticulata, Involves the Kita and Csf1ra Receptor Tyrosine Kinases

Article excerpt

ABSTRACT Males of the guppy (Poecilia reticulata) vary tremendously In their ornamental patterns, which are thought to have evolved in response to a complex interplay between natural and sexual selection. Although the selection pressures acting on the color patterns of the guppy have been extensively studied, little is known about the genes that control their ontogeny. Over 50 years ago, two autosomal color loci, blue and golden, were described, both of which play a decisive role in the formation of the guppy color pattern. Orange pigmentation is absent in the skin of guppies with a lesion in blue, suggesting a defect in xanthophore development. In golden mutants, the development of the melanophore pattern during embryogenesis and after birth is affected. Here, we show that blue and golden correspond to guppy orthologs of colony-stimulating factor 1 receptora (csf1ra; previously called fms) and kita. Most excitingly, we found that both genes are required for the development of the black ornaments of guppy males, which in the case of csf1ra might be mediated by xanthophore-melanophore interactions. Furthermore, we provide evidence that two temporally and genetically distinct melanophore populations contribute to the adult camouflage pattern expressed in both sexes: one early appearing and kita-dependent and the other late-developing and kita-independent. The identification of csf1ra and kita mutants provides the first molecular insights into pigment pattern formation in this important model species for ecological and evolutionary genetics.

THE guppy (Poecilia reticulata) is thought to be among the most color-polymorphic vertebrates (Endler 1983). Male guppies have an outstanding degree of variation in their ornamental patterns, which are shaped by a complex interplay between natural and sexual selection in wild populations. Along with introduction experiments, studies on guppy life-history traits, mate choice behavior, and predator-guppy as well as guppy-environment interactions have demonstrated that guppy populations can adapt rapidly to new environments (for an overview, see Magurran 2005). The guppy is therefore a prime model organism for the study of "evolution in action."

Despite our wealth of knowledge about the ecological importance of coloration, the genes and developmental pathways underlying guppy pigment pattern formation are unknown. Both forward and reverse genetic studies are hampered by the fact that guppies are livebearers with internal fertilization, an average gestation period of 3-4 weeks, and a relatively small brood size (Houde 1997). The genetic basis of sex determination is highly variable within the Poeciliid family, to which the guppy belongs. The guppy itself has incipient X and Y chromosomes that include a non-recombining part (Traut and Winking 2001). Only males develop highly polymorphic ornaments during puberty, which are under hormonal control (Houde 1997). The genetic analysis of male guppy ornaments first attracted attention >80 years ago, when Winge described a total of 18 putative ornamental loci, of which 17 showed sex-linked inheritance and 9 were strictly Y-linked (Winge 1922, 1927). Many more pigment pattern loci, which can be Y-linked, X-linked, XYlinked, or autosomal, have since been described (Lindholm and Breden 2002). Ornamental traits linked to the sex chromosomes are typically expressed only in males, but females can develop some male color patterns when treated with testosterone (Clemens et al. 1966; Lindholm and Breden 2002). An analysis of quantitative trait loci (QTL) has confirmed that most male color traits are controlled by multiple genes, including genes on autosomes (Tripathi et al. 2009b). In contrast to the sex-specific genes, several autosomal color factors behave as ordinary Mendelian recessive genes and are expressed in both sexes (Goodrich et al 1944; Dzwillo 1959; Lindholm and Breden 2002).

The pigment pattern of the guppy consists of three to four different types of neural crest-derived chromatophores: black melanophores, yellow/orange to reddish xanthophores, blue iridescent iridophores, and, possibly, white leukophores (Takeuchi 1976; Tripathi et al. …

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