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Evolutionary Drivers of Electric Signal Diversity

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Electroreception: Fundamental Insights from Comparative Approaches

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 70))

Abstract

The electric signals of weakly electric fishes have seen impressive diversification since the independent origin of electric organs in the ancestors of Gymnotiformes and Mormyroidea approximately 100 million years ago. Whether the primary selective advantage of electric organs lay in their use for communication or for active sampling of the environment is unclear and may be difficult to determine. Several evolutionary innovations in both signal generation and sensory processing appear to have widened the available signal space and thus promoted dramatic radiations. Sensory drive mechanisms are unlikely to have played a major role in the diversification of signals, except for a potential role of flow regimes. Life in faster flow appears to promote faster sensory sampling and thus higher electric organ discharge rates. It seems likely that signal diversification has been driven more strongly by biotic factors. Sexual selection on signal properties and reproductive character displacement appear to have had a strong influence on signal waveform and the associated spectral properties and also on discharge frequency. Diverse evidence suggests that predation by eavesdropping electroreceptive predators has favored the reduction of low-frequency power in the signals. The observation of male signals with strong low-frequency power in sexually dimorphic species is consistent with handicap signals in that they might increase the risk of predation and also the energetic cost of signal generation. Low-frequency male signals may also have been favored by sensory bias of the receiving animals because these signals might also activate the passive, ampullary electrosensory system.

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References

  • Ackerly KL, Krahe R, Sanford CP, Chapman LJ (2018) Effects of hypoxia on swimming and sensing in a weakly electric fish. J Exp biol 221:jeb172130

    Article  PubMed  Google Scholar 

  • Albert JS, Crampton WGR (2005) Diversity and phylogeny of neotropical electric fishes (Gymnotiformes). In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 360–409

    Google Scholar 

  • Alle H, Roth A, Geiger JRP (2009) Energy-efficient action potentials in hippocampal mosy fibers. Science 325:1405–1408

    Article  CAS  PubMed  Google Scholar 

  • Amézquita A, Lima AP, Jehle R, Castellanos L, Ramos O, Crawford AJ, Gasser H, Hödl W (2009) Calls, colours, shape, and genes: a multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biol J Linn Soc 98:826–838

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Arnegard ME, Bogdanovicz SM, Hopkins CD (2005) Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry. Evolution 59(2):324–343

    Article  PubMed  Google Scholar 

  • Arnegard ME, McIntyre PB, Harmon LJ, Zelditch ML, Crampton WGR, Davis JK, Sullivan JP, Lavoué S, Hopkins CD (2010) Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am Nat 176(3):335–356

    Article  PubMed  Google Scholar 

  • Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:133–1145

    Article  Google Scholar 

  • Barbarino-Duque A, Winemiller KO (2003) Dietary segregation among large catfishes of the Apure and Arauca Rivers, Venezuela. J Fish Biol 63:410–427

    Article  Google Scholar 

  • Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DH (eds) Fish physiology. Academic, New York, pp 347–491

    Google Scholar 

  • Bermingham E, Martin AP (1998) Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol 7:499–517

    Article  CAS  PubMed  Google Scholar 

  • Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948

    Article  CAS  PubMed  Google Scholar 

  • Boyle KS, Colleye O, Parmentier E (2014) Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae). Proc R Soc Lond B 281:20141197

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Brenowitz EA (1986) Environmental influences on acoustic and electric animal communication. Brain Behav Evol 28:32–42

    Article  CAS  PubMed  Google Scholar 

  • Carlson BA, Arnegard ME (2011) Neural innovations and the diversification of African weakly electric fishes. Commun Integr Biol 4(6):720–725

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlson BA, Hopkins CD (2004) Stereotyped temporal patterns in electrical communication. Anim Behav 68:867–878

    Article  Google Scholar 

  • Carlson BA, Hasan SM, Hollmann M, Miller DB, Harmon LJ, Arnegard ME (2011) Brain evolution triggers increased diversification of electric fishes. Science 332:583–586

    Article  CAS  PubMed  Google Scholar 

  • Castelló ME, Aguilera PA, Trujillo-Cenóz O, Caputi AA (2000) Electroreception in Gymnotus carapo: pre-receptor processing and the distribution of electroreceptor types. J Exp Biol 203:3279–3287

    PubMed  Google Scholar 

  • Catania KC (2016) Leaping eels electrify threats, supporting Humboldt’s account of a battle with horses. Proc Natl Acad Sci USA 113:6979–6984

    Article  CAS  Google Scholar 

  • Cecil DJ, Buechler DE, Blakeslee RJ (2015) TRMM LIS climatology of thunderstorm occurrence and conditional lightning flash rates. J Clim 28:6536–6547

    Article  Google Scholar 

  • Corcoran AJ, Moss CF (2017) Sensing in a noisy world: lessons from auditory specialists, echolocating bats. J Exp Biol 220:4554–4566

    Article  PubMed  Google Scholar 

  • Crampton WGR (1998a) Effects of anoxia on the distribution, respiratory strategies and electric signal diversity of gymnotiform fishes. J Fish Biol 53(Suppl):307–330

    Article  Google Scholar 

  • Crampton WGR (1998b) Electric signal design and habitat preferences in a species rich assemblage of Gymnotiform fishes from the upper Amazon basin. An Acad Bras Ci 70(4):805–847

    Google Scholar 

  • Crampton WGR (2006) Evolution of electric signal diversity in gymnotiform fishes. Part B. signal design. In: Ladich F, Collin SP, Moller P (eds) Communication in fishes, vol 2. Science Publishers, Enfield, pp 697–731

    Google Scholar 

  • Crampton WGR (2011) An ecological perspective on diversity and distributions. In: Albert JS, Reis RE (eds) Historical biogeography of Neotropical freshwater fishes. University of California Press, Berkeley, pp 165–189

    Chapter  Google Scholar 

  • Crampton WGR, Albert JS (2006) Evolution of electric signal diversity in gymnotiform fishes. Part a. phylogenetic systematics, ecology, and biogeography. In: Ladich F, Collin SP, Moller P (eds) Communication in fishes, vol 2. Science Publishers, Enfield, pp 647–696

    Google Scholar 

  • Crampton WGR, Lovejoy NR, Waddell JC (2011) Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish. Evolution 65(6):1650–1666

    Article  PubMed  Google Scholar 

  • Crampton WGR, Rodríguez-Cattáneo A, Lovejoy NR, Caputi AA (2013) Proximate and ultimate causes of signal diversity in the electric fish Gymnotus. J Exp Biol 216:2523–2541

    Article  CAS  PubMed  Google Scholar 

  • Diaz RJ, Breitburg DL (2009) The hypoxic environment. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia, Fish physiology, vol 27. Elsevier, Amsterdam, pp 1–23

    Chapter  Google Scholar 

  • Dunlap KD (2002) Hormonal and body size correlates of electrocommunication behavior during dyadic interactions in a weakly electric fish, Apteronotus leptorhynchus. Horm Behav 41:187–194

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD, Pelczar PL, Knapp R (2002) Social interactions and cortisol treatment increase the production of aggressive electrocommunication signals in male electric fish, Apteronotus leptorhynchus. Horm Behav 42:97–108

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD, Silva AC, Smith GT, Zakon HH (2017) Weakly electric fish: behavior, neurobiology, and neuroendocrinology. In: Hormones, brain and behavior, vol 2, 3rd edn. Elsevier, Amsterdam, pp 69–98

    Chapter  Google Scholar 

  • Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91

    Article  PubMed  Google Scholar 

  • Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153

    Article  Google Scholar 

  • Enger PS, Szabo T (1968) Effect of temperature on the discharge rates of the electric organ of some gymnotids. Comp Biochem Physiol 27:625–627

    Article  CAS  PubMed  Google Scholar 

  • Engler G, Fogarty CM, Banks JR, Zupanc GKH (2000) Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus: a biophysical and behavioral analysis. J Comp Physiol A 186:645–660

    Article  CAS  PubMed  Google Scholar 

  • Erwin DH (2015) Novelty and innovation in the history of life. Curr Biol 25:R930–R940

    Article  CAS  PubMed  Google Scholar 

  • Falk JJ, ter Hofstede HM, Jones PL, Dixon MM, Faure PA, Kalko EKV, Page RA (2015) Sensory-based niche partitioning in a multiple predator–multiple prey community. Proc R Soc Lond B 282:20150520

    Article  Google Scholar 

  • Feulner PGD, Kirschbaum F, Mamonekene V, Ketmaier V, Tiedemann R (2007) Adaptive radiation in African weakly electric fish (Teleostei: Mormyridae: Campylomormyrus): a combined molecular and morphological approach. J Evol Biol 20:403–414

    Article  CAS  PubMed  Google Scholar 

  • Feulner PGD, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009a) Electrifying love: electric fish use species-specific discharge for mate recognition. Biol Lett 5:225–228

    Article  PubMed  Google Scholar 

  • Feulner PGD, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009b) Magic trait electric organ discharge (EOD). Commun Integr Biol 2(4):329–331

    Article  PubMed  PubMed Central  Google Scholar 

  • Fotowat H, Harrison RR, Krahe R (2013) Statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus. J Neurosci 33:13758–13772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fugère V, Ortega H, Krahe R (2011) Electrical signalling of dominance in a wild population of electric fish. Biol Lett 7:197–200

    Article  PubMed  Google Scholar 

  • Gallant JR, Arnegard ME, Sullivan JP, Carlson BA, Hopkins CD (2011) Signal variation and its morphological correlates in Paramormyrops kingsleyae provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish. J Comp Physiol A 197:799–817

    Article  Google Scholar 

  • Gallant JR, Traeger LL, Volkening JD, Moffett H, Chen PH, Novina CD, Phillips GNJ, Anand R, Wells GB, Pinch M, Güth R, Unguez GA, Albert JS, Zakon HH, Samanta MP, Sussman MR (2014) Genomic basis for the convergent evolution of electric organs. Science 344:1522–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanika S, Kramer B (1999) Electric organ discharges of mormyrid fish as a possible cue for predatory catfish. Naturwissenschaften 86:286–288

    Article  CAS  Google Scholar 

  • Hanika S, Kramer B (2000) Electrosensory prey detection in the African sharptooth catfish, Clarias gariepinus (Clariidae), of a weakly electric mormyrid fish, the bulldog (Marcusenius macrolepidotus). Behav Ecol Sociobiol 48:218–228

    Article  Google Scholar 

  • Hanika S, Kramer B (2005) Intra-male variability of its communication signal in the weakly electric fish, Marcusenius macrolepidotus (South African form), and possible functions. Behaviour 142:145–166

    Article  Google Scholar 

  • Heiligenberg W (1975) Theoretical and experimental approaches to spatial aspects of electrolocation. J Comp Physiol 103:247–272

    Article  Google Scholar 

  • Heiligenberg W (1976) Electrolocation and jamming avoidance in the mormyrid fish Brienomyrus. J Comp Physiol 109:357–372

    Article  Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. MIT Press, Cambridge, MA

    Google Scholar 

  • Heiligenberg W, Baker C, Bastian J (1978) The jamming avoidance response in gymnotoid pulse-species: a mechanism to minimize the probability of pulse-train coincidence. J Comp Physiol 124:211–224

    Article  Google Scholar 

  • Henninger J, Krahe R, Grewe J, Kirschbaum F, Benda J (2018) Statistics of natural communication signals observed in the wild identify important yet neglected stimulus regimes in weakly electric fish. J Neurosci 38:5456–5465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hopkins CD (1972) Sex differences in electric signaling in an electric fish. Science 176:1035–1037

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CD (1973) Lightning as background noise for communication among electric fish. Nature 242:268–270

    Article  Google Scholar 

  • Hopkins CD (1974) Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 272:270–305

    Article  Google Scholar 

  • Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171–207

    Article  Google Scholar 

  • Hopkins CD (1980) Evolution of electric communication channels of mormyrids. Behav Ecol Sociobiol 7:1–13

    Article  Google Scholar 

  • Hopkins CD (1986) Temporal structure of non-propagated electric communication signals. Brain Behav Evol 28:43–59

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CD (1988) Neuroethology of electric communication. Annu Rev Neurosci 11:497–535

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CD (1999a) Design features for electric communication. J Exp Biol 202:1217–1228

    CAS  PubMed  Google Scholar 

  • Hopkins CD (1999b) Signal evolution in electric communication. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, MA, pp 461–491

    Google Scholar 

  • Hopkins CD, Heiligenberg W (1978) Evolutionary designs for electric signals and electroreceptors in gymnotoid fishes of Surinam. Behav Ecol Sociobiol 3:113–134

    Article  Google Scholar 

  • Hopkins CD, Comfort NC, Bastian J, Bass AH (1990) Functional analysis of sexual dimorphism in an electric fish, Hypopomus Pinnicaudatus, order Gymnotiformes. Brain Behav Evol 35(6):350–367

    Article  CAS  PubMed  Google Scholar 

  • Hoskin CJ, Higgie M (2010) Speciation via species interactions: the divergence of mating traits within species. Ecol Lett 13:409–420

    Article  PubMed  Google Scholar 

  • Irwin DE, Thimgan MP, Irwin JH (2008) Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role for stochasticity in signal evolution? J Evol Biol 21:435–448

    Article  CAS  PubMed  Google Scholar 

  • Julian D, Crampton WGR, Wohlgemuth SE, Albert JS (2003) Oxygen consumption in weakly electric Neotropical fishes. Oecol 137:502–511

    Article  Google Scholar 

  • Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) Electroreceptors and other specialized receptors in lower vertrebrates. Springer, Berlin, Heidelberg, pp 147–200

    Chapter  Google Scholar 

  • Kawasaki M (2009) Evolution of time-coding systems in weakly electric fishes. Zool Sci 26(9):587–599

    Article  Google Scholar 

  • Knudsen EI (1974) Behavioral thresholds to electric signals in high frequency electric fish. J Comp Physiol 91:333–353

    Article  Google Scholar 

  • Knudsen EI (1975) Spatial aspects of the electric fields generated by weakly electric fish. J Comp Physiol 99:103–118

    Article  Google Scholar 

  • Kramer B (1997) A field study of African elephantfish (Mormyridae, Teleostei): discharges in Marcusenius macrolepidotus (Peters, 1852) and Petrocephalus catostoma (Günther, 1866) as related to sex. J Afr Zool 111:313–341

    Google Scholar 

  • Kramer B, Kirschbaum F, Markl H (1981) Species specificity of electric organ discharges in a sympatric group of gymnotoid fish from Manaus (Amazonas). In: Szabo T, Czeh G (eds) Sensory physiology of aquatic lower vertebrates, Advances in physiological sciences, vol 31. Akademiai Kiado, Budapest, pp 195–219

    Chapter  Google Scholar 

  • Lamanna F, Kirschbaum F, Ernst ARR, Feulner PGD, Mamonekene V, Paul C, Tiedemann R (2016) Species delimitation and phylogenetic relationships in a genus of African weakly-electric fishes (Osteoglossiformes, Mormyridae, Campylomormyrus). Mol Phylogen Evol 101:8–18

    Article  Google Scholar 

  • Lannoo MJ, Lannoo SJ (1993) Why do electric fishes swim backwards – an hypothesis based on gymnotiform foraging behavior interpreted through sensory constraints. Env Biol Fish 36(2):157–165

    Article  Google Scholar 

  • Lavoué S, Miya M, Arnegard ME, Sullivan JP, Hopkins CD, Nishida M (2012) Comparable ages for the independent origins of electrogenesis in African and South American weakly electric fishes. PLoS One 7:e36287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lewis JE, Gilmour KM, Moorhead MJ, Perry SF, Markham MR (2014) Action potential energetics at the organismal level reveal a trade-off in efficiency at high firing rates. J Neurosci 34:197–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191

    Google Scholar 

  • Lissmann HW (1961) Ecological studies on Gymnotids. In: Chagas C, De Carvalho AP (eds) Bioelectrogenesis. Elsevier, Amsterdam, pp 215–223

    Google Scholar 

  • Lissmann HW, Schwassmann HO (1965) Activity rhythm of an electric fish, Gymnorhamphichthys hypostomus, Ellis. Z Vergl Physiol 51:153–171

    Article  Google Scholar 

  • Lorenzo D, Silva A, Macadar O (2006) Electrocommunication in Gymnotiformes: jamming avoidance and social signals during courtship. In: Ladich F, Collin SP, Moller P (eds) Communication in fishes, vol 2. Science Publishers, Enfield, pp 753–779

    Google Scholar 

  • Lovejoy NR, Lester K, Crampton WGR, Marques FPL, Albert JS (2010) Phylogeny, biogeography, and electric signal evolution of Neotropical knifefishes of the genus Gymnotus (Osteichthyes: Gymnotidae). Mol Phylogen Evol 54:278–290

    Article  Google Scholar 

  • Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14:591–602

    Article  PubMed  Google Scholar 

  • Machnik P, Kramer B (2008) Female choice by electric pulse duration: attractiveness of the males' communication signal assessed by female bulldog fish, Marcusenius pongolensis (Mormyridae, Teleostei). J Exp Biol 211:1969–1977

    Article  PubMed  Google Scholar 

  • Markham MR, McAnelly L, Stoddard PK, Zakon HH (2009) Circadian and social cues regulate ion channel trafficking. PLoS Biol 7(9):e1000203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marrero C, Winemiller KO (1993) Tube-snouted gymnotiform and mormyriform fishes: convergence of a specialized foraging mode in teleosts. Env Biol Fish 38:299–309

    Article  Google Scholar 

  • McAnelly L, Zakon HH (2000) Coregulation of voltage-dependent kinetics of Na+ and K+ currents in electric organ. J Neurosci 20(9):3408–3414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McAnelly L, Zakon HH (2007) Androgen modulates the kinetics of the delayed rectifying K+ current in the electric organ of a weakly electric fish. Dev Neurobiol 67:1589–1597

    Article  CAS  PubMed  Google Scholar 

  • Merron GS (1993) Pack-hunting in two species of catfish, Clarias gariepinus and C. ngamensis, in the Okavango Delta, Botswana. J Fish Biol 43:575–584

    Google Scholar 

  • Moller P (1995) Electric fishes. History and behavior, Fish and fisheries series, vol 17. Chapman and Hall, London

    Google Scholar 

  • Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202:1195–1203

    CAS  PubMed  Google Scholar 

  • Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Q Rev Biol 84(3):253–276

    Article  PubMed  PubMed Central  Google Scholar 

  • Picq S, Alda F, Krahe R, Bermingham E (2014) Miocene and Pliocene colonization of the Central American Isthmus by the weakly electric fish Brachyhypopomus occidentalis (Hypopomidae, Gymnotiformes). J Biogeogr 41:1520–1532

    Article  Google Scholar 

  • Picq S, Alda F, Bermingham E, Krahe R (2016) Drift-driven evolution of electric signals in a Neotropical knifefish. Evolution 70:2134–2144

    Article  PubMed  Google Scholar 

  • Reardon EE, Parisi A, Krahe R, Chapman LJ (2011) Energetic constraints on electric signalling in wave-type weakly electric fishes. J Exp Biol 214:4141–4150

    Article  PubMed  Google Scholar 

  • Reid S (1983) La biologia de los bagres rayados Pseudoplatystoma fasciatum y P. tigrinum en la cuenca del rio Apure – Venezuela. Rev UNELLEZ Ciencia Tecn 1:13–41

    Google Scholar 

  • Rodríguez-Cattáneo A, Aguilera P, Cilleruelo E, Crampton WGR, Caputi AA (2013) Electric organ discharge diversity in the genus Gymnotus: anatomo-functional groups and electrogenic mechanisms. J Exp Biol 216:1501–1515

    Article  PubMed  CAS  Google Scholar 

  • Ryan MJ, Keddy-Hector A (1992) Directional patterns of female choice and the role of sensory biases. Am Nat 139(Suppl):S4–S35

    Article  Google Scholar 

  • Salazar VL, Stoddard PK (2008) Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish, Brachyhypopomus pinnicaudatus. J Exp Biol 211:1012–1020

    Article  PubMed  Google Scholar 

  • Salazar VL, Krahe R, Lewis JE (2013) The energetics of electric organ discharge generation in gymnotiform weakly electric fish. J Exp Biol 216:2459–2468

    Article  CAS  PubMed  Google Scholar 

  • Scheffel A, Kramer B (2006) Intra- and interspecific electrocommunication among sympatric mormyrids in the Upper Zamebzi River. In: Ladich F, Collin SP, Moller P (eds) Communication in fishes, vol 2. Science Publishers, Enfield, pp 733–751

    Google Scholar 

  • Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180

    Google Scholar 

  • Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, Van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626

    Article  CAS  PubMed  Google Scholar 

  • Servedio MR, van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: ‘magic’ but not rare? Trends Ecol Evol 26(8):389–397

    Article  PubMed  Google Scholar 

  • Silva A, Quintana L, Galeano M, Errandonea P, Macadar O (1999) Water temperature sensitivity of EOD waveform in Brachyhypopomus pinnicaudatus. J Comp Physiol A 185:187–197

    Article  Google Scholar 

  • Silva A, Perrone R, Macadar O (2007) Environmental, seasonal, and social modulations of basal activity in a weakly electric fish. Physiol Behav 90:525–536

    Article  CAS  PubMed  Google Scholar 

  • Silva A, Quintana L, Perrone R, Sierra F (2008) Sexual and seasonal plasticity in the emission of social electric signals. Behavioral approach and neural bases. J Physiol (Paris) 102:272–278

    Article  Google Scholar 

  • Smith GT (2013) Evolution and hormonal regulation of sex differences in the electrocommunication behavior of ghost knifefishes (Apteronotidae). J Exp Biol 216:2421–2433

    Article  PubMed  Google Scholar 

  • Smith AR, Proffitt MR, Ho WW, Mullaney CB, Maldonado-Ocampo JA, Alves-Gomes JA, Smith GT (2016) Evolution of electric communication signals in the South American ghost knifefishes (Gymnotiformes: Apteronotidae): a phylogenetic comparative study using a sequence-based phylogeny. J Physiol Paris 110:302–313

    Article  PubMed  PubMed Central  Google Scholar 

  • Stoddard PK (1999) Predation enhances complexity in the evolution of electric fish signals. Nature 400:254–256

    Article  CAS  PubMed  Google Scholar 

  • Stoddard PK (2002) Electric signals: predation, sex, and environmental constraints. In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ (eds) Advances in the study of behavior, vol 31. Academic, San Diego, pp 201–242

    Google Scholar 

  • Stoddard PK, Markham MR (2008) Signal cloaking by electric fish. Bioscience 58:415–425

    Article  PubMed  Google Scholar 

  • Stoddard PK, Salazar VL (2011) Energetic cost of communication. J Exp Biol 214:200–205

    Article  PubMed  Google Scholar 

  • Stoddard PK, Zakon HH, Markham MR, McAnelly L (2006) Regulation and modulation of electric waveforms in gymnotiform electric fish. J Comp Physiol A 192:613–624

    Article  Google Scholar 

  • Stoddard PK, Markham MR, Salazar VL, Allee S (2007) Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus. Physiol Behav 90:11–20

    Article  CAS  PubMed  Google Scholar 

  • Sukhum KV, Freiler MK, Wang R, Carlson BA (2016) The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes. Proc R Soc Lond B 283:20162157

    Article  CAS  Google Scholar 

  • Sullivan JP, Lavoué S, Hopkins CD (2002) Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 56(3):597–616

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JP, Zuanon J, Cox Fernandes C (2013) Two new species and a new subgenus of toothed Brachyhypopomus electric knifefishes (Gymnotiformes, Hypopomidae) from the Central Amazon and considerations pertaining to the evolution of a monophasic electric organ discharge. ZooKeys 327:1–34

    Article  Google Scholar 

  • Turner CR, Derylo M, De Santana D, Alves-Gomes JA, Smith GT (2007) Phylogenetic comparative analysis of electric communication signals in ghost knifefishes (Gymnotiformes: Apteronotidae). J Exp Biol 210:4104–4122

    Article  PubMed  Google Scholar 

  • Vehrencamp SL, Bradbury JW, Gibson RM (1989) The energetic cost of display in male sage grouse. Anim Behav 38:885–896

    Article  Google Scholar 

  • Vélez A, Kohashi T, Lu A, Carlson BA (2017) The cellular and circuit basis for evolutionary change in sensory perception in mormyrid fishes. Sci Rep 7:3783

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Von der Emde G (1999) Active electrolocation of objects in weakly electric fish. J Exp Biol 202:1205–1215

    PubMed  Google Scholar 

  • Waddell JC, Rodríguez-Cattáneo A, Caputi AA, Crampton WGR (2016) Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric knifefish. J Physiol Paris 110:164–181

    Article  PubMed  Google Scholar 

  • Westby GWM (1988) The ecology, discharge diversity and predatory behaviour of gymnotiforme electric fish in the coastal streams of French Guiana. Behav Ecol Sociobiol 22:341–354

    Google Scholar 

  • Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28:156–166

    Article  PubMed  Google Scholar 

  • Zahavi A (1975) Mate selection – a selection for a handicap. J Theoret Biol 53:205–214

    Article  CAS  Google Scholar 

  • Zakon HH, Oestreich J, Tallarovic SK, Triefenbach F (2002) EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiol Paris 96:451–458

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I am grateful to Bernhard Ronacher, Livio Oboti, and Lisa Schilha for critically reading the manuscript and to Jason Gallant, Frank Kirschbaum, Stefan Mucha, Kerri Ackerly, and Sophie Picq for providing some of the recordings used for Fig. 7.1.

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Rüdiger Krahe declares that he has no conflict of interest.

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  1. Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany

    Rüdiger Krahe

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  1. Rüdiger Krahe
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Correspondence to Rüdiger Krahe .

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  1. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Bruce A. Carlson

  2. Department of Psychology, University of Washington, Seattle, WA, USA

    Joseph A. Sisneros

  3. Department of Biology, University of Maryland, College Park, MD, USA

    Arthur N. Popper

  4. Department of Psychology, Loyola University Chicago, Chicago, IL, USA

    Richard R. Fay

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Krahe, R. (2019). Evolutionary Drivers of Electric Signal Diversity. In: Carlson, B., Sisneros, J., Popper, A., Fay, R. (eds) Electroreception: Fundamental Insights from Comparative Approaches. Springer Handbook of Auditory Research, vol 70. Springer, Cham. https://doi.org/10.1007/978-3-030-29105-1_7

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