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

Abstract

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.

Electroreception, electrogenesis and electric signal evolution

“…The myogenic EOs of the Sternopygidae generate EODs with EODfs ranging from 25–1259 Hz (Crampton & Albert, ). The neurogenic EOs of Apteronotidae can generate higher frequency signals, with EODfs ranging from 421–2179 Hz (Crampton & Albert, ; Smith et al ., ).…”

“…Smith et al . () reported considerable variation in chirp structure among apteronotid taxa, particularly among closely related species, suggesting that EOD modulations may play an important role in species recognition and reproductive isolation.…”

“…In the Apteronotidae, a myogenic larval organ is replaced early in development by an adult neurogenic organ in which the electrocytes comprise bundles of elongated spinal motor neuron terminals (Kirschbaum, 1983) and in which the neural circuit that controls the EOD frequency uses only electrical synapses (Smith et al, 2016). In Apteronotus Lacépède 1802 each electromotor axon makes a hairpin bend within the EO and terminates at about the same point that it enters the EO.…”

“…In Brachyhypopomus, these chirps are emitted during courtship behavior, where they can convey sexual receptiveness (Hagedorn, 1988;Perrone et al, 2009;Stoddard, 2002a). Chirps comprising brief frequency or amplitude modulations of the otherwise constant wavetype EOD are also generated in sternopygids (Hagedorn, 1986;Hagedorn & Heiligenberg, 1985) and apteronotids (Hupé & Lewis, 2008;Smith, 2013;Smith et al, 2016;Turner et al, 2007;Zakon et al, 2002) during agonistic interactions and courtship. Chirp structure is sexually dimorphic in all apteronotids and is influenced by both gonadal steroids and neuromodulators (Smith, 2013).…”

“…Here, facultative RCD, operating as a post-speciation process, has evidently driven only minor divergences in EOD waveforms. Based on phylogenetic analyses of wave-type EODs in the Apteronotidae, Smith et al (2016) reported a phylogenetic structuring of many EOD waveform, EODf and chirp modulation traits. However, the authors reported phylogenetic lability of other EOD traits, including among closely related species (Smith et al, 2016).…”