Divergence in androgen sensitivity contributes to population differences in sexual dimorphism of electrocommunication behavior

Abstract

Weakly-electric fish (Apteronotidae) produce highly diverse electrocommunication signals. Electric organ discharges (EODs) vary across species, sexes, and in the magnitude and direction of their sexual dimorphism. Gonadal steroid hormones can modulate EODs, and differences in androgen sensitivity are hypothesized to underlie variation in the degree of sexual dimorphism across species. In this study, we asked whether variation in androgen sensitivity explained variation in sexual dimorphism of EODs within species, at the population level. We examined two populations of black ghost knifefish (Apteronotus albifrons), one from the Orinoco and the other from the Amazon river basin. EOD frequency (EODf) and chirp rates were measured to characterize diversity in sexual dimorphism across populations. The magnitude of sexual dimorphism in EODf differed significantly across populations, and was more pronounced in the Orinoco population than in the Amazon population. Chirp rates were sexually monomorphic in both populations. 11-ketotestosterone (11-kT) was administered over a two-week period to assess population differences in sensitivity to androgens. 11-kT masculinized EODf significantly more in the population with the greater degree of sexual dimorphism. 11-kT had no effect on the sexually monomorphic chirping rates. We conclude that population divergence in androgen sensitivity contributes to variation in sexual dimorphism of EODf in A. albifrons.

Evolution and hormonal regulation of sex differences in the electrocommunication behavior of ghost knifefishes (Apteronotidae)

“…Furthermore, the relationship between androgen effects and sex differences in EODf is consistent across populations within species. 11KT robustly lowers EODf in populations of A. albifrons that are highly sexually dimorphic, whereas EODf is significantly less responsive to 11KT in populations of A. albifrons with smaller sex differences in EODf (Ho et al, 2013). These findings suggest that species diversity in the sexual dimorphism of EODf may evolve in part through the gain or loss of androgen sensitivity, or through the reversal of androgenic effects.…”

“…The genus Apteronotus contains examples of every pattern of sexual dimorphism in EODf: males>females in A. leptorhynchus; males<females in A. albifrons; and no sex difference in A. magdalensis MaldonadoOcampo et al, 2011). Furthermore, Orinoco and Amazonian populations of A. albifrons differ in the magnitude of sex differences in EODf (Ho et al, 2013).…”

“…11KT does not affect chirp rate in A. albifrons, which is sexually monomorphic for chirp rate Ho et al, 2013). In P. hasemani, males produce longer duration chirps than females, and blocking androgen receptors with flutamide demasculinizes chirp duration in males (Petzold and Smith, 2012a).…”

“…In A. albifrons populations from the Orinoco river system, male EODfs are ~200Hz lower than female EODfs, and EODf overlaps little between the sexes. In contrast, sex differences in EODf in Amazonian populations of A. albifrons are modest (~50Hz), with more extensive overlap between the sexes (Ho et al, 2013). In the majority of other apteronotid species that have been studied, EODf does not differ between the sexes (Table2) Maldonado-Ocampo et al, 2011;Petzold and Smith, 2012b;Zhou and Smith, 2006).…”

Sexual dimorphism in the electric knifefish, Gymnorhamphichthys rondoni (Rhamphichthyidae: Gymnotiformes)

“…Secondary sexual dimorphism may also be expressed in communication systems, such as in sound-producing mechanisms (Ali et al 2016;Parmentier et al 2018) or as differences in electrical signal repertoires of male and female electric fishes (Fugere and Krake 2009;Ho et al 2010Ho et al , 2013. Among Neotropical electric fishes of the order Gymnotiformes, the most common forms of sexual dimorphism occur in body size (Hilton and Cox Fernandes 2006; de Santana and Cox Fernandes 2012), snout shape (de Santana 2003; Albert and Crampton 2009;Evans et al 2018), and caudal filament size and shape (Hopkins et al 1990;Giora et al 2008).…”