From Sequence to Spike to Spark: Evo-devo-neuroethology of Electric Communication in Mormyrid Fishes

Abstract

Mormyrid fishes communicate using pulses of electricity, conveying information about their identity, behavioral state, and location. They have long been used as neuroethological model systems because they are uniquely suited to identifying cellular mechanisms for behavior. They are also remarkably diverse, and they have recently emerged as a model system for studying how communication systems may influence the process of speciation. These two lines of inquiry have now converged, generating insights into the neural basis of evolutionary change in behavior, as well as the influence of sensory and motor systems on behavioral diversification and speciation. Here, we review the mechanisms of electric signal generation, reception, and analysis and relate these to our current understanding of the evolution and development of electromotor and electrosensory systems. We highlight the enormous potential of mormyrids for studying evolutionary developmental mechanisms of behavioral diversification, and make the case for developing genomic and transcriptomic resources. A complete mormyrid genome sequence would enable studies that extend our understanding of mormyrid behavior to the molecular level by linking morphological and physiological mechanisms to their genetic basis. Applied in a comparative framework, genomic resources would facilitate analysis of evolutionary processes underlying mormyrid diversification, reveal the genetic basis of species differences in behavior, and illuminate the origins of a novel vertebrate sensory and motor system. Genomic approaches to studying the evo-devo-neuroethology of mormyrid communication represent a deeply integrative approach to understanding the evolution, function, development, and mechanisms of behavior.

Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes

“…African mormyrid fishes are a well-suited model system for relating evolutionary change in sensory systems to species differences in communication (Carlson and Gallant, 2013). Mormyrids communicate by generating a species-specific electric organ discharge (EOD).…”

The transcriptional correlates of divergent electric organ discharges inParamormyropselectric fish

“…Waveform complexity refers to the number of phases present in an EOD, and mormyrid EODs vary in the presence of a small head negative phase (P0). The presence or absence of P0 in the EOD depends on the anatomical configuration of the electrocytes: P0-present (or triphasic) EODs are produced by electrocytes that are innervated on the anterior face and have penetrating stalks (Pa), whereas P0-absent (or biphasic) EODs are produced by electrocytes innervated on the posterior face and lack penetrating stalks (NPp) [42,43,47,48,51,52]. Developmental studies of the adult EO suggest that Pa electrocytes go through a NPp stage before developing penetrations [86,87].…”

“…Within the Mormyridae, triphasic EODs evolved early from biphasic EODs; however, there have been multiple parallel reversions to biphasic EODs across mormyrids and within Paramormyrops [36,43]. Triphasic (P0-present) EODs are produced by electrocytes that are innervated on the anterior face and have penetrating stalks ( Pa , P-type), whereas biphasic (P0-absent) EODs are produced by electrocytes innervated on the posterior face and lack penetrating stalks ( NPp , N-type) (for more details see [42,43,47,48,51,52]). We refer to triphasic EODs as more ‘complex’ than biphasic EODs.…”

The transcriptional correlates of divergent electric organ discharges in Paramormyrops electric fish

“…Within the Mormyridae, triphasic EODs evolved early from biphasic EODs; however, there have been multiple parallel reversions to biphasic EODs across mormyrids and within Paramormyrops [36,43]. Triphasic (P0present) EODs are produced by electrocytes that are innervated on the anterior face and have penetrating stalks (Pa, P-type), whereas biphasic (P0-absent) EODs are produced by electrocytes innervated on the posterior face and lack penetrating stalks (NPp, N-type) (for more details see [42,43,47,48,51,52]). We refer to triphasic EODs as more 'complex' than biphasic EODs.…”