Evolutionary Loss of Male-Specific Coloration Is Associated with the Loss of Androgen Receptor Expression in Skin of Sceloporus Lizards

AbstractHormones can induce trait development in one species yet have no effect on the same trait in a closely related species, but the mechanisms underlying these differences are unclear. Here, we compare two closely related lizard species to explore the cellular mechanisms associated with the evolutionary loss of hormonally mediated ventral coloration. The eastern fence lizard (Sceloporus undulatus) has sexually dimorphic blue and black ventral coloration that develops when maturational increases in androgens induce melanin synthesis in males. The closely related striped plateau lizard (Sceloporus virgatus) has sexually monomorphic white ventral skin that does not produce melanin in response to the same signal. We used immunohistochemistry to localize the androgen receptor (AR) in the skin of both species and to test whether the loss of ventral coloration in S. virgatus corresponds to the loss of AR in the skin. We found that the ventral skin of S. virgatus displays little or no AR staining in the pigment cell layer, potentially explaining the loss of androgen sensitivity in this tissue, relative to the robust AR staining in the same layer of S. undulatus. Based on the location of three markers for melanophores (microphthalmia-associated transcription factor, dopachrome tautomerase, and tyrosinase), AR appears to be present in melanophores in S. undulatus. However, we could not detect these melanophore markers in the skin of S. virgatus. Therefore, the evolutionary loss of ventral coloration may have occurred via the loss of the AR-producing melanophore in mature ventral skin, preventing the development of a male-typical trait and sexual dimorphism in this tissue.