Audience Effects in Territorial Defense of Male Cichlid Fish Are Associated with Differential Patterns of Activation of the Brain Social Decision-Making Network

Abstract

Animals communicate by exchanging signals frequently in the proximity of other conspecifics that may detect and intercept signals not directed to them. There is evidence that the presence of these bystanders modulates the signaling behavior of interacting individuals, a phenomenon that has been named audience effect. Research on the audience effect has predominantly focused on its function rather than on its proximate mechanisms. Here, we have investigated the physiological and neuromolecular correlates of the audience effect in a cichlid fish (Mozambique tilapia, Oreochromis mossambicus). A male was exposed to a territorial intrusion in the presence or absence of a female audience. Results showed that the presence of the female audience increased territorial defense, but elicited a lower androgen and cortisol response to the territorial intrusion. Furthermore, analysis of the expression of immediate early genes, used as markers of neuronal activity, in brain areas belonging to the social decision-making network (SDMN) revealed different patterns of network activity and connectivity across the different social contexts (i.e., audience × intrusion). Overall, these results suggest that socially driven plasticity in the expression of territorial behavior is accommodated in the central nervous system by rapid changes in functional connectivity between nodes of relevant networks (SDMN) rather than by localized changes of activity in specific brain nuclei.

Keywords: aggression; androgens; audience effects; cortisol; immediate early genes; social decision-making network.

Figure 1

Experimental set up: F, Focal tank (glass); I, Intruder tank (glass; placed inside the focal tank) with holes to allow chemical communication; A, Audience tank (glass); 1, permanent barrier to prevent visual communication between intruders and audience; 2, Unidirectional mirror to prevent audience to see and interact with focal males.

Figure 2

Behavioral measurements for the focal fish in each experimental condition. ^*Significant difference for p < 0.05; ^**significant difference for p < 0.01; ^***Significant difference for p < 0.001.

Figure 3

Hormone levels for the focal fish in each experimental condition. (A) Testosterone levels; (B) 11-Ketotestosterone levels; (C) Cortisol levels; ^*significant difference for p < 0.05.

Figure 4

Expression of immediate early genes in brain areas of the SDM network (A) c-fos; (B) and egr-1. ^*Significant difference for p < 0.05; ^**Significant difference for p < 0.01.

Figure 5

Functional connectivity in the SDM network for all the experimental treatments as measured by Pearson correlations between pairs of brain nuclei for c-fos and egr-1. Dm, medial zone of the dorsal telencephalic area; Dl, lateral zone of the dorsal telencephalic area; Vv, ventral nucleus of the ventral telencephalic area; Vs, supracommissural nucleus of the ventral telencephalic area; POA, preoptic area; TA, nucleus anterior tuberis; GC, central gray. ^*Significant correlation for p < 0.05; (.) marginal correlation p < 0.10. Different letters indicate significantly different patterns of IEG expression in brain nuclei between treatments using the QAP correlation test.

Figure 6

Representations of the SDM network for all the experimental treatments clustered by eigenvector centrality treatment and using c-fos and egr-1 as reporters of neuronal activity. Node size indicates eigenvector centrality. Line size indicates the strength of the connection between nodes.