Evolution of androgen receptors contributes to species variation in androgenic regulation of communication signals in electric fishes

Abstract

Hormones and receptors coevolve to generate species diversity in hormone action. We compared the structure and function of androgen receptors (ARs) across fishes, with a focus on ARs in ghost knifefishes (Apteronotidae). Apteronotids, like many other teleosts, have two ARs (ARα and ARβ). ARβ is largely conserved, whereas ARα sequences vary considerably across species. The ARα ligand binding domain (LBD) has evolved under positive selection, and differences in the LBD across apteronotid species are associated with diversity in androgenic regulation of behavior. The Apteronotus leptorhynchus ARα LBD differs substantially from that of the Apteronotus albifrons ARα or the ancestral AR. Structural modeling and transactivation assays demonstrated that A. leptorhynchus ARα cannot bind androgens. We propose a model whereby relative expression of ARα versus ARβ in the brain, coupled with loss of androgen binding by ARα in A. leptorhynchus might explain reversals in androgenic regulation and sex differences in electrocommunication behavior.