Modular genetic control of social status in a cichlid fish.

Abstract

Social hierarchies are ubiquitous in social species and profoundly influence physiology and behavior. Androgens like testosterone have been strongly linked to social status, yet the molecular mechanisms regulating social status are not known. The African cichlid fish <i>Astatotilapia burtoni</i> is a powerful model species for elucidating the role of androgens in social status given their rich social hierarchy and genetic tractability. Dominant <i>A. burtoni</i> males possess large testes and bright coloration and perform aggressive and reproductive behaviors while nondominant males do not. Social status in <i>A. burtoni</i> is in flux, however, as males alter their status depending on the social environment. Due to a teleost-specific whole-genome duplication, <i>A. burtoni</i> possess two androgen receptor (AR) paralogs, <i>ARα</i> and <i>ARβ</i>, providing a unique opportunity to disentangle the role of gene duplication in the evolution of social systems. Here, we used CRISPR/Cas9 gene editing to generate AR mutant <i>A. burtoni</i> and performed a suite of experiments to interrogate the mechanistic basis of social dominance. We find that <i>ARβ,</i> but not <i>ARα</i>, is required for testes growth and bright coloration, while <i>ARα</i>, but not <i>ARβ</i>, is required for the performance of reproductive behavior and aggressive displays. Both receptors are required to reduce flees from females and either AR is sufficient for attacking males. Thus, social status in <i>A. burtoni</i> is inordinately dissociable and under the modular control of two AR paralogs. This type of nonredundancy may be important in facilitating social plasticity in <i>A. burtoni</i> and other species whose social status relies on social experience.