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

The electric communication signals of weakly electric ghost knifefishes (Gymnotiformes: Apteronotidae) provide a valuable model system for understanding the evolution and physiology of behavior. Apteronotids produce continuous wave-type electric organ discharges (EODs) that are used for electrolocation and communication. The frequency and waveform of EODs, as well as the structure of transient EOD modulations (chirps), vary substantially across species. Understanding how these signals have evolved, however, has been hampered by the lack of a well-supported phylogeny for this family. We constructed a molecular phylogeny for the Apteronotidae by using sequence data from three genes (cytochrome c oxidase subunit 1, recombination activating gene 2, and cytochrome oxidase B) in 32 species representing 13 apteronotid genera. This phylogeny and an extensive database of apteronotid signals allowed us to examine signal evolution by using ancestral state reconstruction (ASR) and phylogenetic generalized least squares (PGLS) models. Our molecular phylogeny largely agrees with another recent sequence-based phylogeny and identified five robust apteronotid clades: (i) Sternarchorhamphus+Orthosternarchus, (ii) Adontosternarchus, (iii) Apteronotus+Parapteronotus, (iv) Sternarchorhynchus, and (v) a large clade including Porotergus, 'Apteronotus', Compsaraia, Sternarchogiton, Sternarchella, and Magosternarchus. We analyzed novel chirp recordings from two apteronotid species (Orthosternarchus tamandua and Sternarchorhynchus mormyrus), and combined data from these species with that from previously recorded species in our phylogenetic analyses. Some signal parameters in O. tamandua were plesiomorphic (e.g., low frequency EODs and chirps with little frequency modulation that nevertheless interrupt the EOD), suggesting that ultra-high frequency EODs and "big" chirps evolved after apteronotids diverged from other gymnotiforms. In contrast to previous studies, our PGLS analyses using the new phylogeny indicated the presence of phylogenetic signals in the relationships between some EOD and chirp parameters. The ASR demonstrated that most EOD and chirp parameters are evolutionarily labile and have often diversified even among closely related species.

Hormonal and behavioral correlates of morphological variation in an Amazonian electric fish (Sternarchogiton nattereri: Apteronotidae).

The weakly electric fish from the main channel of the Amazon river, Sternarchogiton nattereri, offers a striking case of morphological variation. Females and most males are toothless, or present only few minute teeth on the mandible, whereas some males exhibit exaggerated, spike-like teeth that project externally from the snout and chin. Androgens are known to influence the expression of sexually dimorphic traits, and might be involved in tooth emergence. In this study we assess the relationship in S. nattereri between morphological variation, 11 ketotestosterone (11-KT) and testosterone (T). We also examine relationships of morphology and androgen levels with electric organ discharge (EOD) frequency, reproductive condition, and seasonality. Our main finding is that male morph categories differed significantly in plasma concentrations of 11-KT, with toothed males showing higher levels of 11-KT than toothless males. By contrast, we did not detect statistical differences in T levels among male morph categories. Reproductive condition, as measured by gonadosomatic indexes (GSI), differed across two sample years, increased as the season progressed, and was higher in toothed males than in non-toothed males. EOD frequency was higher in toothed males than in either toothless males or females. Taken together, our findings suggest that S. nattereri male sexual characters are regulated by 11-KT levels, and that both morphology and androgens interact with reproductive condition and EOD frequency in ways that vary within and across reproductive seasons.