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.

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

Nonapeptides and social behavior in fishes.

Fish populations are increasingly being subjected to anthropogenic changes to their sensory environments. The impact of these changes on inter- and intra-specific communication, and its evolutionary consequences, has only recently started to receive research attention. A disruption of the sensory environment is likely to impact communication, especially with respect to reproductive interactions that help to maintain species boundaries. Aquatic ecosystems around the world are being threatened by a variety of environmental stressors, causing dramatic losses of biodiversity and bringing urgency to the need to understand how fish respond to rapid environmental changes. Here, we discuss current research on different communication systems (visual, chemical, acoustic, electric) and explore the state of our knowledge of how complex systems respond to environmental stressors using fish as a model. By far the bulk of our understanding comes from research on visual communication in the context of mate selection and competition for mates, while work on other communication systems is accumulating. In particular, it is increasingly acknowledged that environmental effects on one mode of communication may trigger compensation through other modalities. The strength and direction of selection on communication traits may vary if such compensation occurs. However, we find a dearth of studies that have taken a multimodal approach to investigating the evolutionary impact of environmental change on communication in fish. Future research should focus on the interaction between different modes of communication, especially under changing environmental conditions. Further, we see an urgent need for a better understanding of the evolutionary consequences of changes in communication systems on fish diversity.

http://redpath-staff.mcgill.ca/hendry/vanderSluijs2011EvolEcol25,623.pdf

Communication in troubled waters: responses of fish communication systems to changing environments

Due to the fish-specific genome duplication event (~320-350 mya), some genes which code for serotonin proteins were duplicated in teleosts; this duplication event was preceded by a reorganization of the serotonergic system, with the appearance of the raphe nuclei (dependent on the isthmus organizer) and prosencephalic nuclei, including the paraventricular and pretectal complexes. With the appearance of amniotes, duplicated genes were lost, and the serotonergic system was reduced to a more complex raphe system. From a comparative point of view, then, the serotonergic system of zebrafish and that of mammals shows many important differences. However, many different behavioral functions of serotonin, as well as the effects of drugs which affect the serotonergic system, seem to be conserved among species. For example, in both zebrafish and rodents acute serotonin reuptake inhibitors (SSRIs) seem to increase anxiety-like behavior, while chronic SSRIs decrease it; drugs which act at the 5-HT1A receptor seem to decrease anxiety-like behavior in both zebrafish and rodents. In this article, we will expose this paradox, reviewing the chemical neuroanatomy of the zebrafish serotonergic system, followed by an analysis of the role of serotonin in zebrafish fear/anxiety, stress, aggression and the effects of psychedelic drugs.

Serotonergic modulation of zebrafish behavior: towards a paradox.

Astrocytes may function as mediators of the impact of noradrenaline on neuronal function. Activation of glial α1-adrenergic receptors triggers rapid astrocytic Ca2+ elevation and facilitates synaptic plasticity, while activation of β-adrenergic receptors elevates cAMP levels and modulates memory consolidation. However, the dynamics of these processes in behaving mice remain unexplored, as do the interactions between the distinct second messenger pathways. Here we simultaneously monitored astrocytic Ca2+ and cAMP and demonstrate that astrocytic second messengers are regulated in a temporally distinct manner. In behaving mice, we found that while an abrupt facial air puff triggered transient increases in noradrenaline release and large cytosolic astrocytic Ca2+ elevations, cAMP changes were not detectable. By contrast, repeated aversive stimuli that lead to prolonged periods of vigilance were accompanied by robust noradrenergic axonal activity and gradual sustained cAMP increases. Our findings suggest distinct astrocytic signaling pathways can integrate noradrenergic activity during vigilance states to mediate distinct functions supporting memory.

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Distinct temporal integration of noradrenaline signaling by astrocytic second messengers during vigilance

Environmental, seasonal, and social modulations of basal activity in a weakly electric fish.

Males and females commonly compete for limited resources. When interaction costs are similar for both sexes and there are no sexual differences in resource value estimation, a non-sex-biased dominance is expected. Moreover, only non-sex-biased assessment of contenders fighting ability (Resource Holding Potential, RHP) should influence contest decisions. To test these predictions, we evaluated non-breeding agonistic intra- and intersexual dyadic interactions in the weakly electric fish, Gymnotus omarorum. During the non-breeding season, resource value is not expected to depend on individuals’ reproductive status and should thus be equal for males and females. In addition, as G. omarorum presents no sexual differences in body size, interaction costs can be considered symmetric between sexes. We confirmed that body size differences, but not individuals’ gender, is the best predictor of dominance. We correlated RHP asymmetries with contest duration and evidenced that body size but not sex influences assessment in intrasexual and intersexual encounters. All dyads tested engaged in agonistic interactions (N = 33) in which a clear dominant emerged. The analysis of conflict phases evidenced the submissive role of electric displays. Electric organ discharge (EOD) interruptions appear early in the contest as an electric hiding attempt, whereas chirps are post-resolution signals of subordinate status. Interestingly, the decision of interrupting the EOD was also influenced by RHP asymmetries, whereas chirping activity was influenced by the intensity of the attacks received. Our results confirm that body size is the best RHP proxy in non-breeding intra- and intersexual contests of this monomorphic species and demonstrated a sequential pattern of submissive signalling by means of two different electric displays.

Non-sex-biased Dominance in a Sexually Monomorphic Electric Fish: Fight Structure and Submissive Electric Signalling

Agonistic behavior has shaped sociality across evolution. Though extremely diverse in types of displays and timing, agonistic encounters always follow the same conserved phases (evaluation, contest and post-resolution) and depend on homologous neural circuits modulated by the same neuroendocrine mediators across vertebrates. Among neuromodulators, serotonin (5-HT) is the main inhibitor of aggression, and arginine vasotocin (AVT) underlies sexual, individual and social context differences in behavior across vertebrate taxa. We aim to demonstrate that a distinct spatio-temporal pattern of activation of the social behavior network characterizes each type of aggression by exploring its modulation by both the 5-HT and AVT systems. We analyze the neuromodulation of aggression between the intermale reproduction-related aggression displayed by the gregarious Brachyhypopomus gauderio and the non-breeding intrasexual and intersexual territorial aggression displayed by the solitary Gymnotus omarorum. Differences in the telencephalic activity of 5-HT between species were paralleled by a differential serotonergic modulation through 1A receptors that inhibited aggression in the territorial aggression of G. omarorum but not in the reproduction-related aggression of B. gauderio. AVT injection increased the motivation towards aggression in the territorial aggression of G. omarorum but not in the reproduction-related aggression of B. gauderio, whereas the electric submission and dominance observed in G. omarorum and B. gauderio, respectively, were both AVT-dependent in a distinctive way. The advantages of our model species allowed us to identify precise target areas and mechanisms of the neuromodulation of two types of aggression that may represent more general and conserved strategies of the control of social behavior among vertebrates.

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Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression.

Brachyhypopomus pinnicaudatus (pulse-type weakly electric fish) is a gregarious species that displays reproductive behavior and agonistic encounters between males only during the breeding season. During social interactions, in addition to its basal electric organ discharge (EOD), fish emit social electric signals (SESs) in the contexts of reproduction and intrasexual aggression. We reproduced natural behavior in laboratory settings: SESs recorded in the field are indistinguishable from those observed in our experimental setup. SESs are nocturnal, change seasonally and exhibit sexual dimorphism. This study provides an exhaustive characterization and classification of SESs produced by males and females during the breeding season. In male-female dyads, males produce accelerations and chirps while females interrupt their EODs. The same SESs are observed in male-male dyads. We present a novel, thorough classification of male chirps into four independent types (A, B, C, and M) based on their duration and internal structure. The type M chirp is only observed in male-male dyads. Chirps and interruptions, both in male-female and male-male dyads, are emitted in bouts, which are also grouped throughout the night. Our data suggest the existence of a sophisticated electric dialog during reproductive and aggressive interaction whose precise timing and behavioral significance are being investigated.

Rossana Perrone

Papers

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

Environmental, seasonal, and social modulations of basal activity in a weakly electric fish.

Non-sex-biased Dominance in a Sexually Monomorphic Electric Fish: Fight Structure and Submissive Electric Signalling

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression.

Social electric signals in freely moving dyads of Brachyhypopomus pinnicaudatus.