Adenylate cyclase 5is required for melanophore and male pattern development in the guppy (Poecilia reticulata)

Abstract

Guppies (Poecilia reticulata) are colorful fish that have attracted the attention of pigmentation researchers for almost a century. Here, we report that the blond phenotype of the guppy is caused by a spontaneous mutation in the guppy ortholog of adenylate cyclase 5 (adcy5). Using double digest restriction site-associated DNA sequencing (ddRADseq) and quantitative trait locus (QTL) mapping, we linked the blond phenotype to a candidate region of 118 kb, in which we subsequently identified a 2-bp deletion in adcy5 that alters splicing and leads to a premature stop codon. We show that adcy5, which affects life span and melanoma growth in mouse, is required for melanophore development and formation of male orange pigmentation traits in the guppy. We find that some components of the male orange pattern are particularly sensitive to loss of Adcy5 function. Our work thus reveals a function for Adcy5 in patterning of fish color ornaments.

The Genome of the Trinidadian Guppy, Poecilia reticulata, and Variation in the Guanapo Population

“…Together, the female reference genome greatly enhances the molecular resources that have been developed for this system [45, 85–87]. The new reference assembly has already helped to determine the molecular basis of color mutations [86] and it has informed comparisons of natural and experimental populations [88]. …”

Magic Traits in Magic Fish: Understanding Color Pattern Evolution Using Reef Fish

“…Zebrafish and medaka are helpful models for combining genetic manipulations with live imaging, and their study has provided new insights on the cellular and molecular mechanisms that drive the development of color patterns [4]. Other fish such as cichlids and guppies have also provided valuable insight into genes and molecular mechanisms underlying specific traits (egg spots and stripes) and various color ornaments [5][6][7].…”

“…Zebrafish and medaka are helpful models for combining genetic manipulations with live imaging, and their study has provided new insights on the cellular and molecular mechanisms that drive the development of color patterns [4]. Other fish such as cichlids and guppies have also provided valuable insight into genes and molecular mechanisms underlying specific traits (egg spots and stripes) and various color ornaments [5][6][7].While mammals only possess melanocytes, the teleost lineage harbors the highest number of pigment cell typesalso called chromatophores (e.g., melanophores, xanthophores, and iridophores) [8]. This diversity can explain the diversity of color and their patterns and implies the involvement of many pigmentation genes.…”

The Colorful Sex Chromosomes of Teleost Fish

“…Although genomic resources have recently become available for the guppy, only the autosomal color loci responsible for the non-sex-specific golden, blue, and blond coloration have been already identified [ 61 , 69 , 91 , 92 , 93 ]. The underlying genes, kita , csf1ra , and adenylate cyclase 5 ( adcy5 ) affect melanocyte and xanthophore development and are most likely indirectly required for male pattern formation [ 61 , 92 ]. The composition of the male-limited and Y-specific pigment pattern loci as iconic as maculatus, however, remains elusive.…”