Hormonal Regulation and the Mechanistic Basis of a Sex‐Limited Color Polymorphism

ABSTRACT The presence of multiple discrete color patterns within a species has captivated evolutionary biologists for more than a century, including cases in which the polymorphism is confined to one sex. The brown anole Anolis sagrei exhibits a female‐limited polymorphism in dorsal patterning, which is controlled by allelic variation at the autosomal CCDC170 locus. Here, we present and test a threshold model that can explain why the polymorphism is female‐limited. We hypothesize that the hormonal environment determines whether allelic variation at the morph‐associated locus is phenotypically manifested, potentially through estrogen‐dependent regulation of CCDC170 and its neighboring gene ESR1 , which are more highly expressed in female than male embryos. By manipulating embryonic estradiol levels, we show that genetic males can be induced to express the polymorphism according to allelic variation at the CCDC170 locus, which is naturally masked in males. Inversely, treating genetic females with fadrozole, which depletes estradiol, leads to monomorphic patterns irrespective of genotype, as in natural males. Using RT‐qPCR on sexual organs, we demonstrate that these effects are accompanied by changes in gene expression levels of CCDC170 and ESR1 in response to estradiol and fadrozole, lending support to the threshold model. Our results suggest that the CCDC170‐ESR1‐ locus is part of a mechanistic link between the morph‐determining and the sex differentiation systems, and provide a causal explanation for the developmental origin of a sex‐limited color polymorphism.