Abstract
Color and color pattern are critical for animal camouflage, reproduction, and defense. Few studies, however, have attempted to identify candidate genes for color and color pattern in squamate reptiles, a colorful group with over 10,000 species. We used comparative transcriptomic analyses between white, orange, and yellow skin in a color-polymorphic species of anole lizard to 1) identify candidate color and color-pattern genes in squamates and 2) assess if squamates share an underlying genetic basis for color and color pattern variation with other vertebrates. Squamates have three types of chromatophores that determine color pattern: guanine-filled iridophores, carotenoid- or pteridine-filled xanthophores/erythrophores, and melanin-filled melanophores. We identified 13 best candidate squamate color and color-pattern genes shared with other vertebrates: six genes linked to pigment synthesis pathways, and seven genes linked to chromatophore development and maintenance. In comparisons of expression profiles between pigment-rich and white skin, pigment-rich skin upregulated the pteridine pathway as well as xanthophore/erythrophore development and maintenance genes; in comparisons between orange and yellow skin, orange skin upregulated the pteridine and carotenoid pathways as well as melanophore maintenance genes. Our results corroborate the predictions that squamates can produce similar colors using distinct color-reflecting molecules, and that both color and color-pattern genes are likely conserved across vertebrates. Furthermore, this study provides a concise list of candidate genes for future functional verification, representing a first step in determining the genetic basis of color and color pattern in anoles.
Highlights
The vertebrate skin has two primary roles: to provide protection against the external environment and to allow organisms to regulate their osmotic balance (Alibardi 2003)
Since squamates use pteridines as pigments (Ortiz and WilliamsAshman 1963; Steffen and McGraw 2007; McLean et al 2017, 2019), we propose that the partial upregulation of the guanine-synthesis pathway in pigment-rich skin could be explained by parts of this pathway associated with the synthesis of guanosine triphosphate (GTP) being involved in the synthesis of pteridine in the yellow and orange dewlap skins (Ziegler 2003)
Xanthophylls scavenged by chromatophores from the bloodstream would undergo ketolation within the chromatophore. This second mechanism allows for the combined action of drosopterins and ketocarotenoids in producing orange or red colors. If this second mechanism holds true, it is likely that one of the two Cytochrome P450 2J family (CYP2J) genes we found to be significantly upregulated in orange skin, CYP2J2 and CYP2J6
Summary
The vertebrate skin has two primary roles: to provide protection against the external environment and to allow organisms to regulate their osmotic balance (Alibardi 2003). The skin is home to pigment-containing and light-scattering cells known as chromatophores (Bagnara and Hadley 1973). The distribution of different types of chromatophores and their light-reflecting molecules produce the colors and color ß The Author(s) 2021. Evol. 13(7). doi:10.1093/gbe/evab110 Advance Access publication 14 May 2021
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