Brain transcriptomics of agonistic behaviour in the weakly electric fish Gymnotus omarorum, a wild teleost model of non-breeding aggression.

Differences in social status are often mediated by agonistic encounters between competitors. Robust literature has examined social status-dependent brain gene expression profiles across vertebrates, yet social status and reproductive state are often confounded. It has therefore been challenging to identify the neuromolecular mechanisms underlying social status independent of reproductive state. Weakly electric fish, Gymnotus omarorum, display territorial aggression and social dominance independent of reproductive state. We use wild-derived G. omarorum males to conduct a transcriptomic analysis of non-breeding social dominance relationships. After allowing paired rivals to establish a dominance hierarchy, we profiled the transcriptomes of brain sections containing the preoptic area (region involved in regulating aggressive behaviour) in dominant and subordinate individuals. We identified 16 differentially expressed genes (FDR < 0.05) and numerous genes that co-varied with behavioural traits. We also compared our results with previous reports of differential gene expression in other teleost species. Overall, our study establishes G. omarorum as a powerful model system for understanding the neuromolecular bases of social status independent of reproductive state.

South American Weakly Electric Fish (Gymnotiformes) Are Long-Wavelength-Sensitive Cone Monochromats.

Losses of cone opsin genes are noted in animals that are nocturnal or rely on senses other than vision. We investigated the cone opsin repertoire of night-active South American weakly electric fish. We obtained opsin gene sequences from genomic DNA of 3 gymnotiforms (Eigenmannia virescens, Sternopygus macrurus, Apteronotus albifrons) and the assembled genome of the electric eel (Electrophorus electricus). We identified genes for long-wavelength-sensitive (LWS) and medium-wavelength-sensitive cone opsins (RH2) and rod opsins (RH1). Neither of the 2 short-wavelength-sensitive cone opsin genes were found and are presumed lost. The fact that Electrophorus has a complete repertoire of extraretinal opsin genes and conservation of synteny with the zebrafish (Danio rerio) for genes flanking the 2 short-wavelength-sensitive opsin genes supports the supposition of gene loss. With microspectrophotometry and electroretinograms we observed absorption spectra consistent with RH1 and LWS but not RH2 opsins in the retinal photoreceptors of E. virescens. This profile of opsin genes and their retinal expression is identical to the gymnotiform's sister group, the catfish, which are also nocturnally active and bear ampullary electroreceptors, suggesting that this pattern likely occurred in the common ancestor of gymnotiforms and catfish. Finally, we noted an unusual N-terminal motif lacking a conserved glycosylation consensus site in the RH2 opsin of gymnotiforms, a catfish and a characin (Astyanax mexicanus). Mutations at this site influence rhodopsin trafficking in mammalian photoreceptors and cause retinitis pigmentosa. We speculate that this unusual N terminus may be related to the absence of the RH2 opsin in the cones of gymnotiforms and catfish.