Status-Dependent Vasotocin Modulation of Dominance and Subordination in the Weakly Electric Fish Gymnotus omarorum

Abstract

Dominant-subordinate status emerges from agonistic encounters. The weakly electric fish, Gymnotus omarorum, displays a clear-cut example of non-breeding territorial aggression. The asymmetry in the behavior of dominants and subordinates is outstanding. Dominants are highly aggressive and subordinates signal submission in a precise sequence of locomotor and electric traits: retreating, decreasing their electric organ discharge rate, and emitting transient electric signals. The hypothalamic neuropeptide arginine-vasotocin (AVT) and its mammalian homolog arginine-vasopressin, are key modulators of social behavior, known to adapt their actions to different contexts. By analyzing the effects of pharmacological manipulations of the AVT system in both dominants and subordinates, we show evidence of distinct status-dependent actions of AVT. We demonstrate an endogenous effect of AVT on dominants' aggression levels: blocking the V1a AVT receptor induced a significant decrease in dominants' attack rate. AVT administered to subordinates enhanced the expression of the electric signals of submission, without affecting subordinates' locomotor displays. This study contributes a clear example of status-dependent AVT modulation of agonistic behavior in teleosts, and reveals distinctive activation patterns of the AVT system between dominants and subordinates.

Keywords: agonistic behavior; electric fish; electric signals; social status; vasotocin modulation.

Figure 1

Electric submission. (A) EOD rate of dominants (white) and subordinates (gray) in pre-contest and post-resolution phases of agonistic encounters. Pre-contest dominants vs. pre-contest subordinates, Mann–Whitney U-test, p = 0.15. Post-resolution dominants vs. subordinates, Mann–Whitney U-test, p = 0.0002. Pre-contest vs. post-resolution dominants, Wilcoxon paired test, p = 0.58. Pre-contest vs. post-resolution subordinates, Wilcoxon paired test, p = 0.001, n = 11 dyads. (B) EOD rate change index. Values around 0 (dotted line in graph) indicate no change in the EOD rate. Index values show a significant decrease in the EOD rate of subordinates whereas the EOD rate of dominants did not change. Index dominants vs. index subordinates, Mann–Whitney U-test, p = 0.03, n = 11 dyads. Box chart symbols: Mean (square), median (line in the middle), 25–75% interquartile range (lower and upper borders), minimum, and maximum values (lower and upper error bars). ^*p < 0.05; ^**p < 0.01.

Figure 2

AVT effects on EOD rate change index. (A) Dominants. Neither AVT nor MC treatment affect the EOD rate change index in dominants. Kruskal–Wallis test, p = 0.46. ncontrol = 11, nAVT = 11, nMC = 6. (B) Subordinates. The EOD rate change index of subordinates after AVT treatment is more pronounced with respect to both saline subordinate controls and MC-treated subordinates. Kruskal–Wallis test, p = 0.04. Post-hoc Dunn test, Control vs. AVT, p = 0.04; Control vs. MC, p = 0.32; AVT vs. MC, p > 0.99. ncontrol = 11, nAVT = 9, nMC = 6. Dotted line indicates no change in EOD rate. Lowercase letters show statistically significance: same letter means non significant differences; different letters mean significant differences.

Figure 3

AVT effects on the rate of emission of transient electric submission signals. (A) Offs. AVT administered to subordinates increases off rate. Control vs. AVT, Mann–Whitney U-test, p = 0.03, ncontrol = 7, nAVT = 7. (B) Chirps. AVT administered to subordinates increases chirp rate. Control vs. AVT, Mann–Whitney U-test, p = 0.04. ncontrol = 7, nAVT = 6. ^*p < 0.05.