Species variation in steroid hormone-related gene expression contributes to species diversity in sexually dimorphic communication in electric fishes

• Published in: Hormones and behavior 2024-08, Vol.164, p.105576, Article 105576
• Main Authors: Proffitt, Melissa R., Smith, G. Troy
• Format: Article
• Language: English
• Subjects: Androgens; Communication; Electric fish; Estrogens; Sexual dimorphism; Steroid metabolism; Steroid receptor cofactors; Steroid receptors
• ISSN: 0018-506X; 1095-6867; 1095-6867
• DOI: 10.1016/j.yhbeh.2024.105576

Sexually dimorphic behaviors are often regulated by gonadal steroid hormones. Species diversity in behavioral sex differences may arise as expression of genes mediating steroid action in brain regions controlling these behaviors evolves. The electric communication signals of apteronotid knifefishes are an excellent model for comparatively studying neuroendocrine regulation of sexually dimorphic behavior. These fish produce and detect weak electric organ discharges (EODs) for electrolocation and communication. EOD frequency (EODf), controlled by the medullary pacemaker nucleus (Pn), is sexually dimorphic and regulated by androgens and estrogens in some species, but is sexually monomorphic and unaffected by hormones in other species. We quantified expression of genes for steroid receptors, metabolizing enzymes, and cofactors in the Pn of two species with sexually dimorphic EODf (Apteronotus albifrons and Apteronotus leptorhynchus) and two species with sexually monomorphic EODf (“Apteronotus” bonapartii and Parapteronotus hasemani). The “A.” bonapartii Pn expressed lower levels of androgen receptor (AR) genes than the Pn of species with sexually dimorphic EODf. In contrast, the P. hasemani Pn robustly expressed AR genes, but expressed lower levels of genes for 5α-reductases, which convert androgens to more potent metabolites, and higher levels of genes for 17β-hydroxysteroid dehydrogenases that oxidize androgens and estrogens to less potent forms. These findings suggest that sexual monomorphism of EODf arose convergently via two different mechanisms. In “A.” bonapartii, reduced Pn expression of ARs likely results in insensitivity of EODf to androgens, whereas in P. hasemani, gonadal steroids may be metabolically inactivated in the Pn, reducing their potential to influence EODf. [Display omitted] •Sex differences in electric organ discharge frequency (EODf) vary across species.•Gonadal steroids act on the pacemaker nucleus (Pn) to produce EODf sex differences.•Hormonal regulation of EODf covaries with sexual dimorphism across species.•The Pn expresses genes for steroid receptors, metabolizing enzymes, and cofactors.•Sexual monomorphism of EODf convergently evolved via different mechanisms.