Meta-analysis of the genetic loci of pigment pattern evolution in vertebrates

Abstract

Vertebrate pigmentation patterns are amongst the best characterised model systems for studying the genetic basis of adaptive evolution. The wealth of available data on the genetic basis for pigmentation evolution allows for meta-analysis of trends and quantitative testing of evolutionary hypotheses. We employed Gephebase, a database of genetic variants associated with natural and domesticated trait variation, to examine trends in how cis-regulatory and coding mutations contribute to vertebrate pigmentation phenotypes, as well as factors that favour one mutation type over the other. We found that studies with lower ascertainment bias identified higher proportions of cis-regulatory mutations, and that cis-regulatory mutations were more common amongst animals harboring a higher number of pigment cell classes. We classified pigmentation traits firstly according to their physiological basis and secondly according to whether they affect colour or pattern, and identified that carotenoid-based pigmentation and variation in pattern boundaries are preferentially associated with cis-regulatory change. We also classified genes according to their developmental, cellular, and molecular functions. We found that genes implicated in upstream developmental processes had greater cis-regulatory proportions than downstream cellular function genes, and that ligands were associated with higher cis-regulatory proportions than their respective receptors. Based on these trends, we discuss future directions for research in vertebrate pigmentation evolution.

The Loci of Insect Phenotypic Evolution

“…Gephebase is up-to-date for all Eukaryotes for studies published prior to 2013. Because of an explosion of relevant studies in recent years, after 2013, we focused mostly on color variation in vertebrates (Gephebase “Trait” Advanced Search field = “Coloration”) [15] and on phenotypic variation in insects (Gephebase “Taxon and synonyms” Advanced Search field = “Insecta”). Compared to our last published report from 2020 [7], Gephebase contains more than 200 additional insect entries.…”

Genetics of continuous colour variation in a pair of sympatric sulphur butterflies

“…A large number of studies have described the Mendelian genetics of colour variation in animals and plants. Various modes of colour production have been investigated, including the synthesis and deposition of melanin, carotenoid, psittacofulvin, and biliverdin pigments in vertebrates (Elkin et al, 2022); melanin, ommochrome, and pterin pigments in insects (Figon and Casas, 2019; Futahashi and Osanai-Futahashi, 2021); and the differentiation of iridescent structural features (Spiewak et al, 2018). These Mendelian colour polymorphisms have often been linked to a set of ‘hotspot’ pigmentation genes that were first described in model organisms, for example MC1R and agouti for melanin variation and BCO2 for carotenoids (Elkin et al, 2022; Gazda et al, 2020).…”

“…Mendelian colour loci have made excellent systems for studying the genetic architecture of variation in natural populations, allowing for preliminary assessments of common classes of mutation; for example, spatial variation in pigmentation is found to be caused by cis -regulatory variation more often than coding variation (Elkin et al, 2022), and signalling molecules such as ligands and their receptors are recurring mutational targets of colour pattern evolution (Martin and Courtier-Orgogozo, 2017). While these findings inform our general understanding of the genetic architecture of other Mendelian traits, most observable traits in wild populations are non-mendelian.…”

Developmental plasticity and variability in the formation of egg-spots, a pigmentation ornament in the cichlidAstatotilapia calliptera

“…Vertebrate pigment patterns are excellent traits in which to address such questions, being extremely diverse both within and between species. Importantly, colour patterns influence a wide range of ecological interactions and are vital for animal adaptation as they can affect courtship behaviour, mate preference, predator avoidance and thermoregulation, among others (Elkin et al, 2022).…”