Holocephalan embryos provide evidence for gill arch appendage reduction and opercular evolution in cartilaginous fishes

Abstract

Chondrichthyans possess endoskeletal appendages called branchial rays that extend laterally from their hyoid and gill-bearing (branchial) arches. Branchial ray outgrowth, like tetrapod limb outgrowth, is maintained by Sonic hedgehog (Shh) signaling. In limbs, distal endoskeletal elements fail to form in the absence of normal Shh signaling, whereas shortened duration of Shh expression correlates with distal endoskeletal reduction in naturally variable populations. Chondrichthyans also exhibit natural variation with respect to branchial ray distribution-elasmobranchs (sharks and batoids) possess a series of ray-supported septa on their hyoid and gill arches, whereas holocephalans (chimaeras) possess a single hyoid arch raysupported operculum. Here we show that the elongate hyoid rays of the holocephalan Callorhinchus milii grow in association with sustained Shh expression within an opercular epithelial fold, whereas Shh is only transiently expressed in the gill arches. Coincident with this transient Shh expression, branchial ray outgrowth is initiated in C. milii but is not maintained, yielding previously unrecognized vestigial gill arch branchial rays. This is in contrast to the condition seen in sharks, where sustained Shh expression corresponds to the presence of fully formed branchial rays on the hyoid and gill arches. Considered in light of current hypotheses of chondrichthyan phylogeny, our data suggest that the holocephalan operculum evolved in concert with gill arch appendage reduction by attenuation of Shhmediated branchial ray outgrowth, and that chondrichthyan branchial rays and tetrapod limbs exhibit parallel developmental mechanisms of evolutionary reduction.

Homology of the Fifth Epibranchial and Accessory Elements of the Ceratobranchials among Gnathostomes: Insights from the Development of Ostariophysans

“…Fusion patterns of these elements vary among elasmobranch groups, but usually involves pharyngobranchials 4 and 5 [13]. A similar pattern of fusion between the posterior epibranchial and pharyngobranchials is found in chimaeroid fishes [64], [65], [84]. This compound element articulates the branchial basket posteriorly to the pectoral girdle through ligaments (most sharks) or even more directly (batoids, particularly myliobatiforms [12], [13], [85], [86]), and is possibly never an entirely separate element (in those taxa in which epibranchial 5 is not fused with the posteriormost pharyngobranchials, it is tightly articulated to them, e.g.…”

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

“…We previously demonstrated that the branchial rays of chondrichthyans also develop under the influence of a Shh-expressing signalling centre (Gillis et al, 2009b(Gillis et al, , 2011, although the precise function of this signalling centre remains unclear. To address this, we have used gene expression analysis, fate-mapping and loss-of-function experiments to investigate the function of gill arch Shh signalling in the little skate (Leucoraja erinacea).…”

First tooth-set outside the jaws in a vertebrate

“…Genome sequencing of the elephant shark (Callorhinchus milii) [3] has raised interest in holocephalans as a model system in comparative evolutionary biology, evolutionary developmental biology and genomics [4 -6]. Extant holocephalans are characterized by a distinctive suite of anatomical specializations [7][8][9][10]; however, we have little appreciation of the deep evolutionary history of this clade and its diagnostic features.…”