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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.

SUBMITTER: Smith AR

PROVIDER: S-EPMC5836322 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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

Smith Adam R AR Proffitt Melissa R MR Ho Winnie W WW Mullaney Claire B CB Maldonado-Ocampo Javier A JA Lovejoy Nathan R NR Alves-Gomes José A JA Smith G Troy GT

Journal of physiology, Paris 20161018 3 Pt B

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 evolv ...[more]

PMID: 27769924

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Project description:A species-level phylogenetic reconstruction of the Neotropical bluntnose knifefish genus Brachyhypopomus (Gymnotiformes, Hypopomidae) is presented, based on 60 morphological characters, approximately 1100 base pairs of the mitochondrial cytb gene, and approximately 1000 base pairs of the nuclear rag2 gene. The phylogeny includes 28 species of Brachyhypopomus and nine outgroup species from nine other gymnotiform genera, including seven in the superfamily Rhamphichthyoidea (Hypopomidae and Rhamphichthyidae). Parsimony and Bayesian total evidence phylogenetic analyses confirm the monophyly of the genus, and identify nine robust species groups. Homoplastic osteological characters associated with diminutive body size and occurrence in small stream habitats, including loss of squamation and simplifications of the skeleton, appear to mislead a phylogenetic analysis based on morphological characters alone-resulting in the incorrect placing of Microsternarchus + Racenisia in a position deeply nested within Brachyhypopomus. Consideration of geographical distribution in light of the total evidence phylogeny indicates an origin for Brachyhypopomus in Greater Amazonia (the superbasin comprising the Amazon, Orinoco and major Guiana drainages), with subsequent dispersal and vicariance in peripheral basins, including the La Plata, the São Francisco, and trans-Andean basins of northwest South America and Central America. The ancestral habitat of Brachyhypopomus likely resembled the normoxic, low-conductivity terra firme stream system occupied by many extant species, and the genus has subsequently occupied a wide range of terra firme and floodplain habitats including low- and high-conductivity systems, and normoxic and hypoxic systems. Adaptations for impedance matching to high conductivity, and/or for air breathing in hypoxic systems have attended these habitat transitions. Several species of Brachyhypopomus are eurytopic with respect to habitat occupancy and these generally exhibit wider geographical ranges than stenotopic species.

Project description:We describe two new, closely related species of toothed Brachyhypopomus (Hypopomidae: Gymnotiformes: Teleostei) from the central Amazon basin and create a new subgenus for them. Odontohypopomus, new subgenus of Brachyhypopomus, is diagnosed by (1) small teeth present on premaxillae; (2) medialmost two branchiostegal rays thin with blades oriented more vertically than remaining three rays; (3) background color in life (and to lesser extent in preservation) distinctly yellowish with head and sides peppered with small, widely spaced, very dark brown stellate chromatophores that greatly contrast with light background coloration; (4) a dark blotch or bar of subcutaneous pigment below the eye; (5) electric organ discharge waveform of very long duration (head-positive phase approx. 2 milliseconds or longer, head-negative phase shorter or absent) and slow pulse repetition rate (3-16 Hz). The type species of the new subgenus, Brachyhypopomus (Odontohypopomus) walteri sp. n., is diagnosed by the following additional character states: (1) subcutaneous dark pigment at base of orbit particularly prominent, (2) body semi-translucent and nearly bright yellow background coloration in life, (3) a biphasic electric organ discharge (EOD) waveform of very long duration (between 3.5 and 4 milliseconds at 25° C) with head-positive first phase significantly longer than second head-negative phase in both sexes. Brachyhypopomus (Odontohypopomus) bennetti sp. n. is diagnosed by two character states in addition to those used to diagnose the subgenus Odontohypopomus: (1) a deep electric organ, visible as large semi-transparent area, occupying approximately 14-17% body depth directly posterior to the abdominal cavity in combination with a short, but deep, caudal filament, and (2) a monophasic, head-positive EOD waveform, approximately 2.1 milliseconds in duration in both sexes. These are the only described rhamphichthyoid gymnotiforms with oral teeth, and Brachyhypopomus bennetti is the first Brachyhypopomus reported to have a monophasic (head-positive) EOD waveform. Unlike biphasic species, the waveform of its EOD is largely unaffected by tail damage from predators. Such injuries are common among specimens in our collections. This species' preference for floating meadow habitat along the major channels of the Amazon River basin may put it at particularly high risk of predation and "tail grazing."

Dataset Information

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

Publications

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

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