Fishing for jaws in early vertebrate evolution: a new hypothesis of mandibular confinement

Abstract

The evolutionary origin of the vertebrate jaw persists as a deeply puzzling mystery. More than 99% of living vertebrates have jaws, but the evolutionary sequence that ultimately gave rise to this highly successful innovation remains controversial. A synthesis of recent fossil and embryological findings offers a novel solution to this enduring puzzle. The Mandibular Confinement Hypothesis proposes that the jaw evolved via spatial confinement of the mandibular arch (the most anterior pharyngeal arch within which the jaw arose). Fossil and anatomical evidence reveals: (i) the mandibular region was initially extensive and distinct among the pharyngeal arches; and (ii) with spatial confinement, the mandibular arch acquired a common pharyngeal pattern only at the origin of the jaw. The confinement occurred via a shift of a domain boundary that restricted the space the mesenchymal cells of the mandibular arch could occupy. As the surrounding domains replaced mandibular structures at the periphery, this shift allowed neural crest cells and mesodermal mesenchyme of the mandibular arch to acquire patterning programs that operate in the more posterior arches. The mesenchymal population within the mandibular arch was therefore no longer required to differentiate into specialized feeding and ventilation structures, and was remodelled into a jaw. Embryological evidence corroborates that the mandibular arch must be spatially confined for a jaw to develop. This new interpretation suggests neural crest as a key facilitator in correlating elements of the classically recognized vertebrate head 'segmentation'.

Development, metamorphosis, morphology, and diversity: The evolution of chordate muscles and the origin of vertebrates

“…According to this idea, the first arch was incorporated into the branchial arches only in more derived chordates, which explains why it is the only arch in vertebrates in which Hox genes are not expressed and do not pattern arch formation (Mallatt, ; see below). Based on a comprehensive review of the recent literature, Miyashita's (; personal communication) “Mandibular Confinement Theory” specifically proposes that the gnathostome jaw evolved by means of developmental spatial confinement of ancestral anterior (oral) chordate structures; due to this confinement these structures acquired/co‐opted, in vertebrates, the genetic/patterning programs that operate in the more posterior arches, thus forming a mandibular arch resembling these arches (Miyashita, ; personal communication). Also falling into the third category is the surprising evidence that appendicularians are the most basal extant urochordates, although the phylogeny of urochordates is still controversial and not all authors accept such a basal position of appendicularians (e.g., Valentine, ; Lemaire, ) (Fig.…”

Homology of the cranial vault in birds: new insights based on embryonic fate-mapping and character analysis

“…We use ‘mandibular stream’ in reference to the rostralmost of the three principal populations in the axolotl, whose cells migrate anterior and posterior to the eye and populate the first (mandibular) oropharyngeal arch [30]. It is equivalent to the ‘trigeminal’ neural crest [26,27], which may comprise distinct preoptic, postoptic and mandibular-arch streams [31,32]. We use ‘hyoid stream’ in reference to the second principal population, which populates the second (hyoid) arch.…”

An atlas of anteriorhoxgene expression in the embryonic sea lamprey head:hox-code evolution in vertebrates

“…The lamprey pharynx comprises 8 pharyngeal arches, which are populated by NC cells migrating in three streams from the hindbrain, broadly equivalent to the three anterior streams of gnathostomes, although a vagal NC stream from the caudal hindbrain appears to be absent in lamprey (Green et al, 2017; Horigome et al, 1999; McCauley and Bronner-Fraser, 2003; Meulemans and Bronner-Fraser, 2002). PA1 is homologous to the mandibular arch of gnathostomes; however, rather than giving rise to the jaw, it forms the velum, a cyclostome-specific piston-like valve involved in ventilating the larval lamprey pharynx (Miyashita, 2016). PA2 is homologous to the hyoid arch of gnathostomes, forming the velar support cartilage, while PA3-8 hold gills, like the posterior pharyngeal arches in aquatic gnathostomes.…”