Building the case for a novel teleost model of non-breeding aggression and its neuroendocrine control

Quintana, Laura; Zubizarreta, Lucía; Jalabert, Cecilia; Batista, Gervasio; Perrone, Rossana; Silva, Ana C.

doi:10.1016/j.jphysparis.2016.11.009

Cited by 31 publications

(45 citation statements)

References 104 publications

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“…the larger fish of the dyad always won the fight). In accordance with previous reports (Batista et al, 2012;Quintana et al, 2016), all the agonistic encounters also showed similar temporal profiles and followed the typical three phases: (1) a short pre-contest of 46.5±43 s; (2) the contest, characterized by highly aggressive displays by both contenders with a duration of 228.5±100 s; and (3) the 10 min post-contest phase, in which dominants, but not subordinates, persisted in attacking while subordinates attempted to flee and emitted submissive electric signals.…”

Section: Agonistic Behaviorsupporting

confidence: 93%

“…The agonistic behavior of Gymnotus omarorum is the best understood example among teleosts of non-breeding territorial aggression (Batista et al, 2012;Jalabert et al, 2015;Quintana et al, 2016). In dyadic contests, the dominant fish defends its territory, while the subordinate fish interrupts its EOD to hide from the dominant one, emits bouts of chirps, and adopts a lower postresolution EOD basal rate than the dominant fish (Batista et al, 2012;Perrone and Silva, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…First, as no glutamatergic actions have been ever demonstrated on the R-cells of the G. omarorum PN (Curti et al, 1999(Curti et al, , 2006, mechanisms underlying subordinate chirps in this species are unlikely to be similar to those demonstrated in Brachyhypopomus. Second, chirps are only emitted by subordinates as the most unambiguous signal of submission (Batista et al, 2012;Quintana et al, 2016). This electric behavior is status dependent (i.e.…”

Section: Introductionmentioning

confidence: 99%

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Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum

Comas

Langevin

Silva

et al. 2019

Journal of Experimental Biology

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South American weakly electric fish (order Gymnotiformes) rely on a highly conserved and relatively fixed electromotor circuit to produce species-specific electric organ discharges (EODs) and a variety of meaningful adaptive EOD modulations. The command for each EOD arises from a medullary pacemaker nucleus composed of electrotonically coupled intrinsic pacemaker and bulbospinal projecting relay cells. During agonistic encounters, Gymnotus omarorum signals submission by interrupting its EOD (offs) and emitting transient high-rate barrages of low-amplitude discharges (chirps). Previous studies in Gymnotiformes have shown that electric signal diversity is based on the segregation of descending synaptic inputs to pacemaker or relay cells and differential activation of the neurotransmitter receptors-for glutamate or γ-aminobutyric acid (GABA)of these cells. Therefore, we tested whether GABAergic and glutamatergic inputs to pacemaker nucleus neurons are involved in the emission of submissive electric signals in G. omarorum. We found that GABA applied to pacemaker cells evokes EOD interruptions that closely resemble natural offs. Although in other species chirping is probably due to glutamatergic suprathreshold depolarization of relay cells, here, application of glutamate to these cells was unable to replicate the emission of this submissive signal. Nevertheless, chirp-like discharges were emitted after the enhancement of excitability of relay cells by blocking an I A-type potassium current and, in some cases, by application of vasotocin, a status-dependent modulator peptide of G. omarorum agonistic behavior. Modulation of the electrophysiological properties of pacemaker nucleus neurons in Gymnotiformes emerges as a novel putative mechanism endowing electromotor networks with higher functional versatility.

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Section: Agonistic Behaviorsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum

Comas

Langevin

Silva

et al. 2019

Journal of Experimental Biology

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“…In line with this, we have found that larger fish hold larger territories (Table 3). Body size is sexually monomorphic in this species and behavioral experiments have shown that agonistic behavior is non-sex-biased (22,39). In this study, we confirmed that non-breeding males and females hold sexually monomorphic territory sizes in the wild, probably to cope with energetic requirements that are not expected to be sexually different during winter.…”

Section: Discussionmentioning

confidence: 86%

“…Previous laboratory results showed that this species presents a remarkably robust non-breeding territorial aggression (initially described in (22)), with well-characterized agonistic behavioral displays including modulations of the electric organ discharge (EOD) to signal submission (35–37) and a dominant phenotype that persists for at least 36 hours (38). Under experimental laboratory conditions, male-male and female-female dyads that display non-breeding territorial behavior have shown no differences in either contest outcome, temporal dynamics of the agonistic encounter, levels of aggression, nor submissive signaling (39). Moreover, the only significant predictor of contest outcome is body size (22), and none of the features of agonistic encounters depends on circulating gonadal hormones (40).…”

Section: Introductionmentioning

confidence: 99%

Seasonal and social factors associated with spacing in a wild territorial electric fish

Zubizarreta

Quintana

Hernández³

et al. 2020

Preprint

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29The expression of territorial behavior in wild species is especially suited to explore how 30 animals integrate individual traits with dynamic environmental and social contexts. In this 31 study, we focused on the seasonal variation of the determinants of territory size in the weakly 32 electric fish Gymnotus omarorum. This species is a seasonal breeder that displays year-33 long territorial aggression, in which female and male dyads exhibit indistinguishable non-34 breeding territorial agonistic behavior and the only significant predictor of contest outcome 35 is body size. We carried out field surveys across seasons that included the identification of 36 individual location, measurements of water physico-chemical variables, characterization of 37 individual morphometric and physiological traits, and their correlation to spatial distribution. 38Although Gymnotus omarorum tolerates a wide range of dissolved oxygen concentration, 39 territory size correlated with dissolved oxygen in both seasons. In the non-breeding season, 40we show that territory size is sexually monomorphic and explained only by body size. In the 41 breeding season, while body size no longer correlated with territory size, evidence of sexual 42 differences in territory size determinants emerged. First, the overall spatial arrangement 43 adopted a sexual bias. Second, territory size depended on gonadal hormones in both sexes, 44which was expected for males, but not previously reported in females. Third, females' 45 territory size correlated with gonadal size and females showed relatively larger territories 46 than males, probably to meet sexually dimorphic energetic requirements. This study 47 provides evidence of seasonal changes in factors correlated with territory size and 48 contributes to the understanding of the mechanisms underlying behavioral plasticity. 49 50 Keywords 51 Non-breeding aggression, sexual dimorphism, Gymnotus omarorum, gonadal steroids 3 52 53

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Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

Borde

Quintana

Comas

et al. 2020

Developmental Neurobiology

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Like stomatogastric activity in crustaceans, vocalization in teleosts and frogs, and locomotion in mammals, the electric organ discharge (EOD) of weakly electric fish is a rhythmic and stereotyped electromotor pattern. The EOD, which functions in both perception and communication, is controlled by a two‐layered central pattern generator (CPG), the electromotor CPG, which modifies its basal output in response to environmental and social challenges. Despite major anatomo‐functional commonalities in the electromotor CPG across electric fish species, we show that Gymnotus omarorum and Brachyhypopomus gauderio have evolved divergent neural processes to transiently modify the CPG outputs through descending fast neurotransmitter inputs to generate communication signals. We also present two examples of electric behavioral displays in which it is possible to separately analyze the effects of neuropeptides (mid‐term modulation) and gonadal steroid hormones (long‐term modulation) upon the CPG. First, the nonbreeding territorial aggression of G. omarorum has been an advantageous model to analyze the status‐dependent modulation of the excitability of CPG neuronal components by vasotocin. Second, the seasonal and sexually dimorphic courtship signals of B. gauderio have been useful to understand the effects of sex steroids on the responses to glutamatergic inputs in the CPG. Overall, the electromotor CPG functions in a regime that safeguards the EOD waveform. However, prepacemaker influences and hormonal modulation enable an enormous versatility and allows the EOD to adapt its functional state in a species‐, sex‐, and social context‐specific manners.

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Building the case for a novel teleost model of non-breeding aggression and its neuroendocrine control

Cited by 31 publications

References 104 publications

Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum

Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum

Seasonal and social factors associated with spacing in a wild territorial electric fish

Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

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