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. 2012 Sep;139(17):3142-6.
doi: 10.1242/dev.084046. Epub 2012 Jul 25.

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

J Andrew Gillis  1 , Melinda S Modrell, R Glenn Northcutt, Kenneth C Catania, Carl A Luer, Clare V H Baker
Affiliations

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

J Andrew Gillis et al. Development. 2012 Sep.

Abstract

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, whereas 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.

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Figures

Fig. 1
Fig. 1. Lateral line placodal origin of skate ampullary organs and neuromasts.
(A) Wholemount immunostaining for parvalbumin-3 (Pv3) in L. erinacea embryos reveals a cephalic network of (B) mechanosensory neuromasts and (C) electrosensory ampullary organs. In order to test the lateral line placodal origin of neuromasts and ampullary organs, we fate-mapped the anterodorsal or anteroventral lateral line placodes. These placodes were recognizable as (D) ectodermal thickenings caudal to the eye and dorsal to the mandibular and hyoid arches, respectively, which (E) express the transcription co-factor gene Eya4. (F) An embryo in which the anterodorsal and anteroventral lateral line placodes were focally labelled with DiI. (G) In an embryo in which the anterodorsal lateral line placode was labelled, DiI was observed at 14 days post-injection in the supraorbital lateral line primordium (black arrows), far from the original injection site (*). In embryos with DiI-labelled anterodorsal and/or anteroventral lateral line placodes, the distribution of DiI-positive cells at 60-70 days post-injection recapitulated the normal distribution of (H-J) cephalic neuromasts, ampullary pores and (K-M) ampullary organs. ad, anterodorsal lateral line placode; ao, ampullary organ; ap, ampullary tubule pore; av, anteroventral lateral line placode; e, eye; nm, neuromast; ot, otic vesicle; so, supraorbital lateral line primordium. Scale bars: A,H,K: 2.5 mm; B-C,J,M: 0.5 mm; D-E: 0.5 mm; G: 0.8 mm.
Fig. 2
Fig. 2. Lateral line placodal origin of sensory receptor cells, support cells and canal cells in skate ampullary organs and cephalic neuromasts.
(A) A ventral view of the head, illustrating the elongation of the sensory ridge of the anterodorsal lateral line placode that will give rise to the infraorbital neuromasts and closely associated ampullary organs. (B) A lateral view of the head, illustrating the elongation of the sensory ridge of the anterodorsal lateral line placode as it passes rostral and ventral to the eye (where it will run medial to the more laterally situated infraorbital line), giving rise to the supraorbital neuromasts and closely associated ampullary organs. (C) Electrosensory ampullary organs (black arrows) are clustered within the dermis, and each sensory ampulla opens externally via a long jelly-filled ampullary canal (*). (D) Mechanosensory neuromasts are distributed within a continuous network of epithelial canals. Immunohistochemical localization of parvalbumin-3 (Pv3) in (E) ampullary organs and (F) neuromasts reveals small clusters of sensory receptor cells nested among non-sensory support cells. (G) Electrosensory hair cells and (H) mechanosensory hair cells both express Eya4, an established marker of the developing lateral line system. Fate-mapping of the anterodorsal lateral line placode of L. erinacea by DiI injection reveals a placodal origin of (I) the Pv3-positive sensory hair cells, non-sensory support cells and (J) canal cells of electrosensory ampullary organs, and (K) the Pv3-positive sensory hair cells, canal cells and (L) non-sensory support cells of mechanosensory neuromasts. Images in panels I,J,K,L are all from different individuals. ap, ampullary tubule pore; e, eye; io, infraorbital sensory ridge; m, mouth; nm, neuromast; olf, olfactory organ; so, supraorbital sensory ridge. Scale bars: A: 125 µm; B: 50 µm; C-D: 24 µm; E-L: 10 µm.
Fig. 3
Fig. 3. Lateral line placodal origin of both sensory receptor cells and support cells in skate trunk neuromasts.
(A) The skate posterior lateral line placode is recognizable as an elongated ectodermal thickening dorsal to the pharyngeal arches. (B) This placode elongates caudally along the entire length of the trunk, forming (C) a distinct ridge in the epidermis. (D) The posterior lateral line placode expresses the transcription co-factor gene Eya4. (E) L. erinacea embryos in which the posterior lateral line placode was labelled with DiI show (F-H) DiI-positive cells organized in a pattern that recapitulates the normal distribution of (I) parvalbumin-3 (Pv3)-positive trunk mechanosensory neuromasts. (J) Immunohistochemical localization of Pv3 in trunk neuromasts reveals small clusters of sensory hair cells nested among non-sensory support cells; (K) these sensory hair cells also express Eya4. (L) The presence of DiI in trunk neuromast Pv3-positive sensory hair cells as well as in non-sensory support cells confirms the posterior lateral line placodal origin of these cell types in L. erinacea. m, middle lateral line placode; pcf, pectoral fin; pvf, pelvic fin; st, supratemporal lateral line placode; nm, neuromast; pllp, posterior lateral line placode. Scale bars: A,C-E: 250 µm; B: 100 µm; F: 5 mm; G-I: 500 µm; J-L: 10 µm.
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