Adaptive Reptile Color Variation and the Evolution of the McIr Gene

Abstract

Abstract. The wealth of information on the genetics of pigmentation and the clear fitness consequences of many pigmentation phenotypes provide an opportunity to study the molecular basis of an ecologically important trait. The melanocortin-1 receptor (Mc1r) is responsible for intraspecific color variation in mammals and birds. Here, we study the molecular evolution of Mc1r and investigate its role in adaptive intraspecific color differences in reptiles. We sequenced the complete Mc1r locus in seven phylogenetically diverse squamate species with melanic or blanched forms associated with different colored substrates or thermal environments. We found that patterns of amino acid substitution across different regions of the receptor are similar to the patterns seen in mammals, suggesting comparable levels of constraint and probably a conserved function for Mc1r in mammals and reptiles. We also found high levels of silent-site heterozygosity in all species, consistent with a high mutation rate or large long-term effective population size. Mc1r polymorphisms were strongly associated with color differences in Holbrookia maculata and Aspidoscelis inornata. In A. inornata, several observations suggest that Mc1r mutations may contribute to differences in color: (1) a strong association is observed between one Mc1r amino acid substitution and dorsal color; (2) no significant population structure was detected among individuals from these populations at the mitochondrial ND4 gene; (3) the distribution of allele frequencies at Mc1r deviates from neutral expectations; and (4) patterns of linkage disequilibrium at Mc1r are consistent with recent selection. This study provides comparative data on a nuclear gene in reptiles and highlights the utility of a candidate-gene approach for understanding the evolution of genes involved in vertebrate adaptation.

Systematics and phylogeography of a threatened tortoise, the speckled padloper

“…Colour variation of the dorsal body surface has often been interpreted as an adaptation for crypsis (Rosenblum, 2005), and experimental studies have shown that substrate matching strongly influences avian predation rates (Kaufman, 1974;Hoekstra, 2006). Colour polymorphism in reptiles may be caused by genetic variability, for example, variation in the Mc1r gene (Rosenblum, Hoekstra & Nachman, 2004), or may be a consequence of an ontogenetic change in response to environmental stimuli (Dunn, 1982;Rosenblum, 2005). found major inconsistencies between morphological taxa and mtDNA clades of the T. graeca complex and reported a strong correlation between substrate and tortoise colour in some regions.…”

Dorsal colour pattern variation in Eurasian mountain vipers (genus Montivipera): A trade-off between thermoregulation and crypsis

“…Although variation in colour pattern in populations of the MRC could reflect an underlying level of biodiversity within this group, but reptile coloration has long been studied as an example of adaptive evolution (e.g. Cott, 1940;Rosenblum et al, 2004). So far there has not been a comprehensive study performed on the adaptive nature of intra-and interpopulation variation in colour pattern of the MRC.…”

Variation in the evolutionary integration of melanism with behavioral and physiological traits in Xiphophorus variatus

“…A number of well known case studies have demonstrated links between ecology, phenotypic variation, and underlying genetic mechanisms [e.g., Drosophila and Heliconius, reviewed in Kronforst et al (2012)]. For example, ecological selection for matching background color in pocket mice living on dark lava rock compared to light sand (Nachman et al 2003) and similarly for skin coloration of White Sands lizards on different substrates (Rosenblum et al 2004) has driven genetic changes underlying pigmentation variation between populations and species. Research on pigmentation has increasingly turned its focus to the evolution and maintenance of integrated phenotypes.…”