Modular genetic control of social status in a cichlid fish

Abstract

AbstractSocial 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 Astatotilapia burtoni is a powerful model species for elucidating the role of androgens in social status given their rich social hierarchy and genetic tractability. Dominant A. burtoni males possess large testes, bright coloration, and perform aggressive and reproductive behaviors while non-dominant males do not. Social status in A. burtoni is in flux, however, as males alter their status depending on the social environment. Due to a teleost-specific whole-genome duplication, A. burtoni possess two androgen receptor (AR) paralogs, ARα and ARβ, 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 A. burtoni and performed a suite of experiments to interrogate the mechanistic basis of social dominance. We find that ARβ, but not ARα, is required for testes growth and bright coloration, while ARα, but not ARβ, 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 A. burtoni is inordinately dissociable and under the modular control of two AR paralogs. This type of non-redundancy may be important in facilitating social plasticity in A. burtoni and other species whose social status relies on social experience.Significance StatementSocial rank along a hierarchy determines physiological state and behavioral performance. A ubiquitous feature of social hierarchies is the communication of rank through non-physical signaling systems (e.g., coloration) and aggression, traits that correlate with the reproductive status of an individual. Despite the links identified between social status, physiology, and behavior, the molecular basis of social status is not known. Here, we genetically dissect social status in the African cichlid fish Astatotilapia burtoni using CRISPR/Cas9 gene editing. We show that two distinct androgen receptor (AR) genes control social status in a highly modular manner. This type of coordination of social status may be fundamental across species that rely on social information to optimally guide physiology and behavior.