Androgen signaling regulates spawning behavior and inhibits parental care in male Astatotilapia burtoni

Abstract

Across the animal kingdom, there is a striking diversity in sex-specific behaviors, from aggression, to mating, and parental care. What makes males and females behave differently? A key challenge in neuroethology is to identify the mechanisms and neural circuits that mediate these sex differences. Sex-specific behaviors are regulated by internal factors, such as hormones, as well as sensory inputs, including pheromonal olfactory cues. While sex hormones such as androgens and estrogens have conserved roles in sexual differentiation, our understanding of how sex hormone receptors function across species is sparse. Similarly, our understanding of how pheromones guide sex-specific behaviors is constrained to a few vertebrate models, limiting our knowledge of conserved mechanisms. In this dissertation, I study the olfactory and hormonal control of sex-specific behaviors in the African cichlid, Astatotilapia burtoni, a model species with highly sexually dimorphic social behaviors. We previously showed A. burtoni males are robustly attracted to pheromones released by fertile females. Here, I use single nucleus RNA-sequencing to identify key populations of olfactory neurons that mediate male attraction to fertile females while also inhibiting parental care. In A. burtoni, the two androgen receptor genes, arα and arβ, have key, dissociable roles in the regulation of male-typical behavior, but our understanding of how and where these two genes function in the stereotyped male mating pattern is incomplete. Using in situ hybridization, I detect androgen receptor mRNA expression in the brain and olfactory epithelium, indicating that androgens act at sensory and central levels of neural processing to coordinate male behaviors. I use CRISPR-generated arβ mutant and arα/β double mutant male cichlids to investigate the role of arβ in the control of male mating behavior. I show that arβ mutants are less likely to advance through the stereotyped phase of spawning behavior. I also uncover a gain in parental care in arβ and arα/β double mutant males, in which the males rapidly retrieve eggs and mouthbrood them, behaviors normally only performed by females. My work suggests a model in which sexually dimorphic behavior in vertebrates is shaped by hormonal regulation of shared neural substrates.