Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes

Abstract

Summary Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, while a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI-tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.

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.…”

A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

“…CM-DiI fate-mapping experiments were carried out as described (Gillis et al, 2012). All animal work complied with protocols approved by the Institutional Animal Care and Use Committee at the MBL.…”

“…Sections of CM-DiI-labelled embryos were counterstained with DAPI. In situ hybridisation experiments for L. erinacea Shh (GenBank accession number EF100667) and Ptc2 (GenBank accession number EF100663) were performed as described (Gillis et al, 2012).…”