Pigment cell organization and genetic analysis of color pattern formation in the guppy (Poecilia reticulata)

Abstract

The evolution of vertebrate pigment patterns has attracted much attention for decades. The pigment pattern of male guppies (Poecilia reticulata) is exceptionally variable and subject to strong natural and sexual selection. Previous studies suggested that a plethora of color genes located on the autosomes and the sex chromosomes of the guppy direct color pattern formation in this small livebearer. In my thesis, I present evidence that the ornaments of male guppies consist of three types of pigment cells, black melanophores, orange xanthophores, and blue reflective iridophores and that iridophores are present in each of the male color ornaments. Further, I show that early Kita-dependent and late Kita-independent melanophores are essential for the formation of the guppy female and male net-like reticulate pattern. I also found that most xanthophores of the guppy require the ancient paralog of Kita, Colony-stimulating factor 1 receptor a (Csf1ra), for their development. Analysis of the phenotypes of kita and csf1ra mutant males demonstrated that both gene products are required for male pigment pattern formation. In the case of Csf1ra, I suggest that this is mediated by interactions between melanophores and xanthophores. Identification of blond as the guppy ortholog of adenylate cyclase 5 (adcy5) and analysis of the effects of the adcy5 loss-of-function mutation revealed that all melanophores of the guppy require Adcy5 for their differentiation. The mutation in adcy5 also strongly affects most of the male-specific orange ornaments, whose formation probably depends on cues given by the melanophores to the xanthophores. Taken together, my work revealed that Kita-, Csf1ra-, and Adcy5-signaling are fundamentally important for guppy pigment pattern formation. The identification of the function of these autosomal pigmentation genes represents an important step towards understanding the genetics and evolution of guppy coloration, especially as modifications in the Kita and Csf1ra pathways have been shown to be involved in the evolution of the color patterns of other vertebrates.