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

Abstract

SummaryThe ghost knifefishes (family Apteronotidae) are one of the most successful and diverse families of electric fish. Like other weakly electric fish, apteronotids produce electric organ discharges (EODs) that function in electrolocation and communication. This review highlights the diversity in the structure, function and sexual dimorphism of electrocommunication signals within and across apteronotid species. EOD frequency (EODf) and waveform vary as a function of species, sex and/or social rank. Sex differences in EODf are evolutionarily labile; apteronotid species express every pattern of sexual dimorphism in EODf (males>females; males<females; males=females). The direction and magnitude of sex differences in EODf are correlated across species and populations with the responsiveness of EODf to androgens and/or estrogens, which suggests that sex differences evolve through gains and/or losses of hormone sensitivity. During social interactions, apteronotids also modulate their EODs to produce motivational signals known as chirps. Chirp structure differs markedly across species, and many species produce two or more discrete chirp types with potentially different functions. The structure of chirps is sexually dimorphic in all apteronotid species, and chirping is influenced by gonadal steroids and by neuromodulators. Encoding of chirps by the electrosensory system depends on the social context created by the interactions of the EODs of signalers and receivers. Electrosensory systems may thus influence the evolution of signal structure and function, and neuromodulators may coordinately shape the production and reception of electrocommunication signals depending on social context.

Evolution of electric communication signals in the South American ghost knifefishes (Gymnotiformes: Apteronotidae): A phylogenetic comparative study using a sequence-based phylogeny

“…They continuously produce high-frequency electric organ discharges (EODs) that act as communication signals conveying information about species identity, sex, and social rank. Both the frequency and the waveform of these fishes’ EODs vary across apteronotid species, and in some species, the EOD is sexually dimorphic and may vary as a function of body size and/or dominance (Smith, 2013). These fish also transiently modulate EOD frequency (EODf) and/or amplitude to produce chirps that act as motivational signals during courtship or aggression.…”

“…These fish also transiently modulate EOD frequency (EODf) and/or amplitude to produce chirps that act as motivational signals during courtship or aggression. Like EODs, chirps also vary substantially across apteronotid species (Smith, 2013). EODs and chirps thus provide an ideal model for studying the evolution of communication.…”

Co-adaptation of electric organ discharges and chirps in South American ghost knifefishes (Apteronotidae)

“…1; Hagedorn & Heiligenberg, 1985; Larimer & MacDonald, 1968). Thus, the EOD is a continuous badge of identity, whereas chirps are transient indicators of motivational state (Smith, 2013). EODs and chirps have relatively simple structures that can be easily recorded, analyzed, manipulated, synthesized, and played back.…”

“…The complicated dynamic created by the co-evolution of EODs and chirps is one potential explanation for the existence of an enormous degree of variation in signal structure between sexes and across different species of weakly electric knifefish (Smith, 2013; Turner et. al, 2007; Zakon & Dunlap, 1999).…”

Electric fishes: neural systems, behaviour and evolution

“…These processes demand interdisciplinary approaches and integration across different levels of biological organization. Weakly electric fishes facilitate these sorts of integrative studies, ranging from the control of electric behaviours and sensory processing by hormones and neuromodulators (Gavassa et al, 2013;Silva et al, 2013;Smith, 2013;Toscano Marquez et al, 2013;Markham, 2013) to neurogenesis (Dunlap, 2013) and tissue regeneration (Unguez, 2013). In the upcoming years we expect the experimental advantages of electric fish to be exploited to also address questions of higherorder brain function, such as those related to cognition.…”