The evolution and development of vertebrate lateral line electroreceptors

Abstract

SummaryElectroreception is an ancient vertebrate sense with a fascinating evolutionary history involving multiple losses as well as independent evolution at least twice within teleosts. We review the phylogenetic distribution of electroreception and the morphology and innervation of electroreceptors in different vertebrate groups. We summarise recent work from our laboratory that has confirmed the homology of ampullary electroreceptors in non-teleost jawed vertebrates by showing, in conjunction with previously published work, that these are derived embryonically from lateral line placodes. Finally, we review hypotheses to explain the distribution of electroreception within teleosts, including the hypothesis that teleost ampullary and tuberous electroreceptors evolved via the modification of mechanosensory hair cells in lateral line neuromasts. We conclude that further experimental work on teleost electroreceptor development is needed to test such hypotheses.

Denticle-embedded ampullary organs in a Cretaceous shark provide unique insight into the evolution of elasmobranch electroreceptors

“…Indeed, the latter are more similar to macro-ampullae, the most common type of ampullae of Lorenzini found in modern elasmobranchs (Andres and von Düring 1988), by the fact that both have a larger receptor organ connected to the skin surface by a well- developed canal or tubule (Meyer and Seegers 2012). Overall, the exquisitely preserved specimen described here offers the possibility to examine the electroreceptor morphology of "C." amonensis and thereby provides the first palaeontological hint of the developmental and evolutionary links existing between the electrosensory (ampullae) and mechanosensory (lateral line neuromasts) systems (Gillis et al 2012;Baker et al 2013).…”

“…However, this unique mineralized structure and its embedded ampullary receptor devoid of canal strongly differ from the typical ampullae of Lorenzini (i.e., macro-ampullae sensu Andres and von Düring 1988) found in living elasmobranchs. In the latter, the alveolar sacs are located in the dermis and are connected to a more or less elongate canal opening in a single somatic pore on the skin surface (Andres and von Düring 1988;Jørgensen 2005;Gillis et al 2012;Baker et al 2013), between the surrounding, generally unmodified, placoid scales (Reif 1985;McKenzie et al 2014). The electrosensory ampullary system of "C." amonensis is characterized by small-sized (∼250 μm) receptor organs, similar in diameter to the mini-ampullae described in many freshwater rays (e.g.…”

“…These denticle-covered pit organs are a derived feature found mainly in galeomorph sharks, including all lamniforms except Mitsukurina (Reif 1985;Peach and Rouse 2004). It is now known that ampullary organs arise from lateral line placodes in the cartilaginous fish clade (Gillis et al 2012;Baker et al 2013). Hence, it is proposed here that the highly specialized dermal denticles of "C." amonensis are developmentally derived by early fusion from the modified denticles that cover the superficial neuromast cavities of the mechanosensory lateral line system of many neoselachian sharks (Fig.…”

“…Although elasmoid scales of teleost fishes arise from mesoderm (Lee et al 2013;Mongera and Nüsslein-Volhard 2013;Shimada et al 2013), it cannot be excluded that both mesoderm-derived and neural crest-derived mesenchymal cells contribute to the formation of more ancestral types of scales such as tooth-like placoid scales of cartilaginous fishes (Green et al 2015). As mentioned above, electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes (Gillis et al 2012;Baker et al 2013), not neural-crest derived as previously reported (Freitas et al 2006). In teleost fishes, a bone remodeling process occurs in unison with the development of the lateral line canal system (Wada et al 2014).…”

Whole-organism cellular gene-expression atlas reveals conserved cell types in the ventral nerve cord of Platynereis dumerilii

“…Cell types represent evolutionary units, defined as "sets of cells that change in evolution together, partially independent of other cells, and evolutionarily more closely related to each other than to other cells" (2). One important focus of interest is the evolution of neurons and nervous systems, with several studies comparing sensory neurons (3)(4)(5)(6), interneurons (7), or motor neurons (8,9). The starting point for these comparisons has been the observation that molecular regions in the developing nervous system are conserved from medial to lateral, between vertebrate and fly (10), and vertebrate and annelids (9) (Fig.…”