Embryonic origin and serial homology of gill arches and paired fins in the skate, Leucoraja erinacea.

Victoria A Sleight,J Andrew Gillis

doi:10.7554/elife.60635

Abstract

Paired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.

Highlights

It was classically proposed that the paired fins of jawed vertebrates evolved by transformation of a gill arch – a theory stemming largely from Gegenbaur’s (Gegenbaur, 1878) interpretation of a shared anatomical ground plan between the gill arch and pectoral fin skeletons of cartilaginous fishes
When considered alongside lineage tracing data from bony fishes, our findings allow us to infer an ancestral mesodermal contribution to the jawed vertebrate gill arch skeleton (Figure 4A), with the transition from neural crest-derived to mesodermally-derive skeletogenic mesenchyme occurring gradually, and spanning the region of the posterior pharyngeal arches (Figure 4B)
Our fate mapping experiments point to a neural crest origin of the mandibular and hyoid arch skeleton, a dual NC/mesodermal origin of the gill arch skeleton and an exclusively mesodermal origin of the pectoral fin skeleton in cartilaginous fishes (Figure 4C)

Summary

Introduction

It was classically proposed that the paired fins of jawed vertebrates evolved by transformation of a gill arch – a theory stemming largely from Gegenbaur’s (Gegenbaur, 1878) interpretation of a shared anatomical ground plan between the gill arch and pectoral fin skeletons of cartilaginous fishes (sharks, skates and rays) (reviewed by Coates, 1994; Coates, 2003). The jaw, hyoid and gill arch skeleton (or, in amniotes, their derivatives, the jaw, auditory ossicles and laryngeal skeleton) arises from a series of transient, bilaterally paired pharyngeal arches that form on the sides of the embryonic head (Gillis et al, 2012a; Graham et al, 2019), while the paired fins or limbs of jawed vertebrates arise as buds that project from the embryonic trunk (Tickle, 2015). Though, the distinct embryonic origins of the gill arch and paired fin skeletons may not hold true: mesodermal contributions to the posterior pharyngeal skeleton have been demonstrated in tetrapods, but are much less widely appreciated than those from neural crest. Cell lineage tracing using quail-chick chimaeras and viral labelling have revealed that the avian cricoid and arytenoid laryngeal cartilages derive from lateral mesoderm, and not neural crest

Methods

Results

Conclusion