Evolution of electric communication signals in the South American ghost knifefishes (Gymnotiformes: Apteronotidae): A phylogenetic comparative study using a sequence-based phylogeny
Introduction
Communication signals transmit information about signalers and adaptively influence the behavior of receivers (Bradbury and Vehrencamp, 2011, Endler, 1993). Comparatively studying communication systems can elucidate processes that guide the evolution of animal behavior such as selective constraints on signal structure, evolution of sensory systems, and sexual selection (Endler, 1992, Endler et al., 2005, Ryan, 1998, Ryan and Rand, 1993). As with many behavioral traits, understanding the evolution of communication signals relies on both (i) an accurate and well-resolved phylogeny; and (ii) accurate quantitative data on signal parameters across a sufficient number of species within sampled clades. Phylogenetic comparative methods have been powerful tools for reconstructing the evolution of communication signals and sensory capacities in model systems where large datasets are available, such as visual displays in lizards (Ord and Martins, 2006), calls in frogs (Tobias et al., 2011, Wilczynski et al., 2001), and plumage coloration in birds (Hofmann et al., 2006, Odom et al., 2014).
The South American knifefishes (Order Gymnotiformes) are a diverse clade of weakly-electric teleost fishes distributed widely throughout Central and South America. These fish produce and detect weak electric fields, which are used for the identification of nearby objects, prey detection, and communication (Bullock et al., 2005, Hagedorn and Heiligenberg, 1985, Hopkins, 1972, Hopkins, 1974). The neural circuits that control the production and reception of these signals are well described (Berman and Maler, 1999, Carr and Maler, 1986, Heiligenberg et al., 1996, Metzner, 1999, Smith, 1999), and the signals are diverse both across and within species (Crampton, 1998, Crampton and Albert, 2006, Crampton et al., 2011, Hopkins, 1988, Kramer et al., 1981, Turner et al., 2007). Gymnotiform fishes have consequently become an established neuroethological model for comparative studies of the evolution and physiology of communication, sex differences, and sensory biology (Dulka, 1997, Dulka and Ebling, 1999, Hopkins, 1988, Krahe and Fortune, 2013, Krahe and Maler, 2014, Meyer et al., 1987, Smith, 1999, Turner et al., 2007, Zakon et al., 1999).
The ghost knifefishes (Apteronotidae) are the most speciose family of gymnotiform fishes (Crampton and Albert, 2006), with more than 90 species in 15 genera. They are only electric fishes whose electric organs are composed of nervous, rather than muscle, tissue (Bennett, 1971). 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. 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. Most previous attempts to reconstruct the evolution of electric signals within the Apteronotidae, however, were hampered by relatively poorly resolved and conflicting phylogenies (Turner et al., 2007). Here, we present a new molecular phylogeny for Apteronotidae, which we compare to previous phylogenetic hypotheses, including a recent gymnotiform tree proposed by Tagliacollo et al. (2016).
The aims of this study were (1) to use concatenated molecular sequence data from two mitochondrial genes and one nuclear gene to further test hypothesized relationships among apteronotid species; and (2) to use the resulting phylogeny and a comprehensive and updated dataset of EOD and chirp parameters to examine the evolution and co-evolution of EODs and chirps in this family.
Section snippets
Taxon sampling
We analyzed molecular sequence data from tissue samples of 84 individuals representing 32 apteronotid species in 13 genera. These samples also included members of Apteronotus sensu stricto and ‘Apteronotus’, which represent two clades from the likely polyphyletic genus Apteronotus (Albert and Crampton, 2005, Crampton and Albert, 2006, de Santana, 2002, Triques, 2005). Species identifications, tissue sources, voucher accession numbers, and NCBI accession numbers for gene sequences are listed in
Apteronotid phylogeny based on concatenated sequences
Statistics for total alignment lengths, variable site number, and overall mean genetic distances for each gene are shown in Table S3. The overall genetic distances for the mitochondrial genes CytB and COI are similar to each other. RAG2 has a much lower overall mean genetic distance among sequences than CytB and COI, which is consistent with the slower rate of evolution of nuclear vs. mitochondrial genes (Brown et al., 1979).
The topologies of individual gene trees were largely consistent, but
Comparison of phylogenies
The concatenated phylogeny generated in this study (Fig. 2) agrees with the sequence- and morphology-based phylogeny proposed by Tagliacollo et al. (2016) in all major respects. In particular, we confirm their conclusions that (i) the genus Adontosternarchus is a sister clade to all apteronotids besides Sternarchorhamphus + Orthosternarchus, (ii) ‘Apteronotus’ species form a clade with the genus Porotergus, and (iii) Sternarchorhynchus is a sister group to a large clade encompassing Porotergus + ‘
Funding
This work was supported by NSF IOS 0950721 to GTS, INPA’s internal funding Grant #12307 to JAG, and an NSERC Discovery Grant to NRL. Support for ARS and WWH was provided by the Common Themes in Reproductive Diversity training program at Indiana University (NIH-NIHCD 5T32HD049336-10). This research was supported in part by Lilly Endowment, Inc., through its support for the Indiana University Pervasive Technology Institute, and in part by the Indiana METACyt Initiative. The Indiana METACyt
Acknowledgements
JAMO is grateful to TWAS-CNPq Postgraduate Fellowships program for support during this project. Special thanks to Mark Sabaj-Perez at the Academy of Natural Sciences in Philadelphia (ANSP) for providing sample tissues and species identifications. Support for processing tissue and DNA samples for sequencing was provided by the core laboratory of the Center for the Integrative Study of Animal Behavior (CISAB) at Indiana University.
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