Electroreception, electrogenesis and electric signal evolution

Abstract

Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by c. 16% of fish species, an animal uses low‐frequency‐tuned ampullary electroreceptors to detect microvolt‐range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak (< 1 V) electric‐organ discharge (EOD) and detecting distortions in the EOD‐associated field using high‐frequency‐tuned tuberous electroreceptors. Tuberous electroreceptors also detect the EODs of neighbouring fishes, facilitating electrocommunication. Several other groups of elasmobranchs and teleosts generate weak (< 10 V) or strong (> 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic–electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non‐adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal‐receptor matching.

Electroreception in marine fishes: chondrichthyans

“…The freshwater sensitivity is commensurate with that of the obligate freshwater P. motoro , which can detect voltages as weak as 5 μV cm −1 (Harris et al, ). This suggests that a reduced sensitivity and detection range of electrical stimuli in freshwater species (Crampton, ) occurs due to the lower conductivity and higher resistivity of fresh water compared with seawater and not the morphological adaptations of thicker skin and shorter ampullary canals seen in obligate freshwater elasmobranchs (Harris et al, ).…”

“…These aspects are fundamental to understanding how electrosensitive species might respond to electrical changes in the marine environment. The review complements that of electroreception in freshwater fishes by Crampton (2019), which provides a comprehensive state of knowledge regarding the evolution of electroreception, particularly active electroreception and electric signal generation in electric fishes. For further specific reviews on chondrichthyan electroreception, readers are referred to Collin and Whitehead (2004), Gardiner et al (2012), Kajiura et al (2010), Tricas and Sisneros (2004) and Wilkens and Hofmann (2005).…”

Electric and magnetic senses in marine animals, and potential behavioral effects of electromagnetic surveys

“…Another source of natural electric fields is living organisms. Organisms constantly generate electric fields during their life processes for example during cell membrane transport, muscle contractions and nerve cell communication (Crampton 2019). The characteristics of the generated electric fields depend on the taxa, position and activity of the animal, and typically range from 2 000 -100 000 nV/cm at a very close distance (Haine et al 2001).…”

Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

“…In pulse‐type fish, in contrast, the interval between EODs is much larger than its duration and the electric discharge consists of a series of discrete, rhythmic and stereotyped beats. The functional division of gymnotiform into pulse and wave types is likely associated with ancient divergences in niche occupancy that shaped the evolution of signal diversity among this group (Crampton, ). However, phylogenetic analysis of morphological and molecular data indicate that pulse‐ and wave‐type families can be more closely related than families of pulse‐type fish (Crampton, ).…”