Climate and genetic structure shape the heterogeneous color distribution of the Guinan toad-headed lizard (Phrynocephalus guinanensis)

As one of the most conspicuous aspects of organismal diversity, animal coloration has attracted scientific interests for centuries. However, the evolutionary drivers that have facilitated the coloration variation remain poorly understood, particularly for species exhibiting multiple color traits. The Guinan toad-headed lizard (Phrynocephalus guinanensis) provides an excellent model to investigate this question, which has a restricted distribution in the Mugetan Desert region, and shows polymorphic ventral coloration including black and sexually dichromatic traits (red in males and green in females). Using standardized spectrophotometry and digital imaging analysis, we quantified the coloration for 137 individuals from 15 populations of this species. Generalized linear models incorporating bioclimatic variables and genetic structure showed that the distributions of the three colors were significantly associated with climatic factors, respectively, especially for the black that could be substantially explained by mean annual temperature potentially reflecting its function in thermoregulation. Nevertheless, the patterns of red and green were also influenced by the population genetic structure for both males and females, implying their role in sexual selection. Our study indicated that both climate and genetic structure have shaped the heterogeneous color distribution of this species, providing novel insights into how animal coloration evolves and diversifies.