Context-dependent chemosensory signaling, aggression, and neural activation patterns in gravid female African cichlid fish

Abstract

Social animals must constantly assess their environment to make appropriate behavioral decisions. The use of various sensory modalities is imperative in this process and it is hypothesized that the highly conserved brain nuclei comprising the social decision making network (SDMN) integrates social information with an animal's internal state to elicit behavioral responses. Here, we used the highly social African cichlid fish, Astatotilapia burtoni, to investigate whether reproductively-receptive (gravid) females show contextual chemosensory signaling, social behaviors, and neural activation patterns within the SDMN. We exposed gravid females to different social contexts: 1) dominant male (inter-sexual reproductive); 2) mouth brooding (non-receptive) female, and 3) gravid female (intra-sexual aggressive); 4) juvenile fish (low social salience); and 5) empty compartment (control). By injecting females with a blue dye to visualize urine pulses, we found that gravid females show context-dependent urination, exhibiting higher urination rates in the presence of dominant males (reproductive context) and mouth brooding females (aggressive contexts). Further, gravid females show contextual aggression with increased aggressive displays toward mouth brooding females compared to other gravid females. Using in situ hybridization to quantify cells expressing the immediate early gene cfos as a measure of neural activation, we also show that certain regions of the SDMN in gravid females are differentially activated after exposure to high compared to low social salience contexts. Coupled with previous reports, these results demonstrate true chemosensory communication in both sexes of a single fish species, as well as reveal the neural substrates mediating intra- and inter-sexual social behaviors in females.