Differential serotonergic modulation of two types of aggression in weakly electric fish

Abstract

Agonistic aggression has provided an excellent framework to study how conserved circuits and neurochemical mediators control species-specific and context-dependent behavior. The principal inhibitory control upon aggression is serotonin (5-HT) dependent, and the activation of 5-HT1A receptors is involved in its action. To address whether the serotonergic system differentially regulates different types of aggression, we used two species of weakly electric fish: the solitary Gymnotus omarorum and the gregarious Brachyhypopomus gauderio, which display distinctive types of aggression as part of each species' natural behavioral repertoire. We found that in the reproduction-related aggression displayed by B. gauderio after conflict resolution, the serotonergic activity follows the classic pattern in which subordinates exhibit higher 5-HT levels than controls. After the territorial aggression displayed by G. omarorum, however, both dominants and subordinates show lower 5-HT levels than controls, indicating a different response of the serotonergic system. Further, we found interspecific differences in basal serotonin turnover and in the dynamic profile of the changes in 5-HT levels from pre-contest to post-contest. Finally, we found the expected reduction of aggression and outcome shift in the territorial aggression of G. omarorum after 8-OH-DPAT (5-HT1A receptor agonist) administration, but no effect in the reproduction-related aggression of B. gauderio. Our results demonstrate the differential participation of the serotonergic system in the modulation of two types of aggression that we speculate may be a general strategy of the neuroendocrine control of aggression across vertebrates.

Extra-gonadal steroids modulate non-breeding territorial aggression in weakly electric fish

“…Territorial aggression of G. omarorum in intra-and intersexual interactions during the non-breeding season has been described previously (Batista et al, 2012;Silva et al, 2013;Zubizarreta et al, 2012Zubizarreta et al, , 2015. Accordingly, in this study, surgically-identified males displayed typical agonistic behavior in dyadic interactions (Fig.…”

“…The electric signals depend on a very well-known and tractable neural circuit (Caputi et al, 2005;Stoddard, 2002), and the relative simplicity of this electromotor circuit offers important operational advantages for studying the neuroendocrine control of behavior. The non-breeding territorial aggression of G. omarorum constitutes a clear example of non-sex biased territorial aggression, unique among teleosts, in which we can precisely identify the phases of the agonistic encounter, the emergence of the dominance-subordination status, levels of aggression and an orderly sequence of submissive electric displays (Batista et al, 2012;Silva et al, 2013;Zubizarreta et al, 2012Zubizarreta et al, , 2015. The original description of the non-breeding agonistic behavior of G. omarorum showed that size asymmetry (but not individual sex nor dyad composition) predicted contest outcome (Batista et al, 2012).…”

“…The weakly electric fish Gymnotus omarorum, a well-established neuroethological model (reviewed in Caputi et al, 2005;Lorenzo et al, 2006;Silva et al, 2002), shows inter-and intrasexual nonbreeding territorial aggression (Batista et al, 2012;Zubizarreta et al, 2012Zubizarreta et al, , 2015 modulated by neuropeptides (Silva et al, 2013) and social context and monoamines (Zubizarreta et al, , 2015. The electric organ discharge (EOD) plays a key role in communication, signaling submission during aggressive encounters and subordinate status once rank is determined (Batista et al, 2012;Silva et al, 2013).…”

Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni

“…In the golden hamster, AVP facilitated offensive aggression in males, which can be blocked by pretreatment with a selective serotonin re-uptake inhibitor (SSRI) (Delville et al, 1996;Ferris and Delville, 1994) or 5-HTR 1A agonist (Ferris et al, 1999). A direct interaction between serotonergic and vasopressin neurons in the anterior hypothalamus of hamsters was described (Ferris et al, 1997) and the possibility of a similar case in the weakly electric fish Gymnotus omarorum was recently speculated (Zubizarreta et al, 2012). Using in situ hybridization, Greenwood et al demonstrated that in subordinate A. burtoni, AVT expression is higher in parvocellular neurons compared with dominant males (Greenwood et al, 2008).…”

Behavioral ecology, endocrinology and signal reliability of electric communication

“…The EOD of B. gauderio could serve as an indicator of body length because the amplitude of the signal physically depends on the length of the electric organ, which runs the length of the fish's body (Curtis and Stoddard, 2003;Hopkins, 1999;Hopkins et al, 1990). Moreover, body length is key for mate choice and male-male interactions, as longer males are more attractive to females (Curtis and Stoddard, 2003) and are more likely to win agonistic encounters (Salazar, 2009;Zubizarreta et al, 2012). Therefore, receivers should pay particular attention to any information about body length coded in the signal.…”