The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective

Abstract

According to current phylogenetic theory, both electroreceptors and electric organs evolved multiple times throughout the evolution of teleosts. Two basic types of electroreceptors have been described: ampullary and tuberous electroreceptors. Ampullary‐type electroreceptors appeared once in the common ancestor of the Siluriformes+Gymnotiformes (within the superorder Ostariophysi), and on two other occasions within the superorder Osteoglossomorpha: in the African Mormyriformes and in the African Notopteriformes. Tuberous receptors are assumed to have evolved three times; all within groups that already possessed ampullary receptors. With the exception of a single catfish species, for which studies are still lacking, all fish with tuberous electroreceptors also have an electric organ. Tuberous electroreceptors are found in the two unrelated electrogenic teleost lineages (orders Gymnotiformes and Mormyriformes) and in one non‐electrogenic South American catfish species (order Siluriformes). Electric organs evolved eight times independently among teleosts: five of them among the ostariophysans (once in the gymnotiform ancestor and in four siluriform lineages), once in the common ancestor of Mormyriformes, and in two uranoscopids. With the exception of two uranoscopid genera, for which no electroreceptive capabilities have been discovered so far, all electric organs evolved as an extension of a pre‐existing electroreceptive (ampullary) condition. It is suggested that plesiomorphic electric organ discharges (EODs) possessed a frequency spectrum that fully transgressed the tuning curve of ampullary receptors, i.e. a signal such as a long lasting monophasic pulse. Complex EOD waveforms appeared as a derived condition among electric fish. EODs are under constant evolutionary pressure to develop an ideal compromise between a function that enhances electrolocation and electrocommunication capabilities, and thereby ensures species identity through sexual and behavioural segregation, and minimizes the risk of predation.