Electroreception in early vertebrates: survey, evidence and new information

Abstract

Electroreception is widespread in living vertebrates, and is often considered to be a primitive vertebrate character. However, the early evolution of electroreception remains unclear. A variety of structures in early vertebrate fossils have been put forward as potential electroreceptors, but these need to be reassessed in light of the now substantial literature on electroreceptors in living vertebrates. Here we review the evidence for all putative electroreceptors in early vertebrates, and provide new information from CT scans. In the jawless osteostracans, the pore canal system in the dermal skeleton and the lateral and dorsal fields do not resemble electroreceptors in living species. Nevertheless, the presence of a recurrent ramus of the anterior lateral line nerve in osteostracans suggests that electroreceptors were present, by comparison with lampreys. In placoderms, cutaneous sense organs on arthrodire cheek plates are possible electroreceptors. CT data shows that the orientation of these pits is anomalous for electroreceptors, and intimately associated with bone growth. A newly identified type of cheek pit, for which the term 'Young's apparatus' is introduced, is known from only two arthrodire specimens. It is closely associated with the underlying jaw joint, but its precise function is unknown. In osteichthyans, the 'pore group' clusters of early sarcopterygians may have housed electroreceptors. CT data from Devonian lungfish support this interpretation, showing internal morphology consistent with electroreceptors, and innervation via the rostral tubuli underlying the dermal bone of the snout. The early osteichthyan Ligulalepis has pit structures which may be electroreceptors, and were possibly innervated by lateral line nerves. Specialized electroreceptor systems, including elaborated 'pore group' pits in Devonian lungfish and rostral organs in the earliest coelacanths, show that electroreception may have had an important role in niche specialization in early vertebrates. Finally, fossil data does not support the hypothesis that vertebrate hard tissues initially evolved to shield electroreceptors.

The emergence of a complex pore‐canal system in the dermal skeleton ofTremataspis(Osteostraci)

“…Similarly, the true functional role of the pore‐canal system in Tremataspis has remained unclear, with suggestions ranging from mucous canals (Stensiö, 1932) or extensions of the lateral lines (Bölau, 1951; Denison, 1947, 1966) to a system for electroreceptors (Thomson, 1977). King et al (2018) reviewed and discussed these previous suggestions and refuted an electroreceptive role for the pore‐canal system, leaning more toward a mechanoreceptive function similar to lateral lines. This view, however, was not shared by O'Shea et al (2019), who thoroughly investigated the three‐dimensional (3D) histology of a single specimen of Tremataspis mammillata and discussed its potential development and function.…”

Evidence of chitin in the ampullae of Lorenzini of chondrichthyan fishes

“…S1F). This could suggest that the use of chitin in electrosensory organs evolved in the ancestor to all cartilaginous fishes, perhaps in the placoderms [6]. A more detailed treatment of chitin synthase genes within Chondrichthyes will be reported elsewhere.…”

Evidence of Chitin in the Ampullae of Lorenzini of Chondrichthyan Fishes

“…S1F and are representative of both elasmobranch and holocephalan lineages. The presence of chitin within the AoL of both subclasses (and in diverse orders within the Elasmobranchii) suggests that this condition evolved in the ancestor to all cartilaginous fishes, perhaps in the placoderms [6]. A more detailed treatment of chitin synthase genes within Chondrichthyes will be reported elsewhere.…”