Gill developmental program in the teleost mandibular arch

Abstract

Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws.

Pre-mandibular pharyngeal pouches in early non-teleost fish embryos

“…In Cambrian yunnanozoans, that supposedly possess an ancestral vertebrate pharyngeal arch condition [78], the rostral-most head is occupied by a pharyngeal domain extending into a prominent snout in a clearly pre-oral position (figure 5 c ), reminiscent of the situation in early non-teleost fish embryos (figure 5 b ). The ancestral vertebrate condition, as revealed in yunnanozoans, is also consistent with the conventional hypothesis that every pharyngeal arch was once equipped with gills as a typical branchial arch [7,8,12,78], which has recently been supported by findings of rudimentary mandibular gills in cartilaginous and teleost fishes [79,80]. Apparently, during early vertebrate evolution, fully pharyngeal metameric organization of our ancestors became reduced, in concert with extensive changes specifically in the pre-chordal part of the head, including emancipation of the mouth and jaw apparatus, and formation of the rostral brain [9–11].…”

The paradise fish, an advanced animal model for behavioral genetics and evolutionary developmental biology

“…To clarify the true evolutionary origins of the labyrinth apparatus, it will be also important to perform fate‐mapping experiments and compare the gene expression programs that are activated during the formation of the LO and SBC with those observed during standard gill development. It is noteworthy that the modular activation of the gill developmental program can be also observed during the development of the pseudobranch itself (Thiruppathy et al, 2022). As demonstrated recently, this structure, which is derived from the mesenchyme of the mandibular arch, does not only show anatomical resemblance to gill filaments, but also shares a gene expression program with those (Hirschberger & Gillis, 2022; Thiruppathy et al, 2022).…”

“…It is noteworthy that the modular activation of the gill developmental program can be also observed during the development of the pseudobranch itself (Thiruppathy et al, 2022). As demonstrated recently, this structure, which is derived from the mesenchyme of the mandibular arch, does not only show anatomical resemblance to gill filaments, but also shares a gene expression program with those (Hirschberger & Gillis, 2022; Thiruppathy et al, 2022).…”