Pattern and polarity in the development and evolution of the gnathostome jaw: Both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula

Abstract

The acquisition of jaws constitutes a landmark event in vertebrate evolution, one that in large part potentiated their success and diversification. Jaw development and patterning involves an intricate spatiotemporal series of reciprocal inductive and responsive interactions between the cephalic epithelia and the cranial neural crest (CNC) and cephalic mesodermal mesenchyme. The coordinated regulation of these interactions is critical for both the ontogenetic registration of the jaws and the evolutionary elaboration of variable jaw morphologies and designs. Current models of jaw development and evolution have been built on molecular and cellular evidence gathered mostly in amniotes such as mice, chicks and humans, and augmented by a much smaller body of work on the zebrafish. These have been partnered by essential work attempting to understand the origins of jaws that has focused on the jawless lamprey. Chondrichthyans (cartilaginous fish) are the most distant group to amniotes within extant gnathostomes, and comprise the crucial clade uniting amniotes and agnathans; yet despite their critical phylogenetic position, evidence of the molecular and cellular underpinnings of jaw development in chondrichthyans is still lacking. Recent advances in genome and molecular developmental biology of the lesser spotted dogfish shark, Scyliorhinus canicula, make it ideal for the molecular study of chondrichthyan jaw development. Here, following the 'Hinge and Caps' model of jaw development, we have investigated evidence of heterotopic (relative changes in position) and heterochronic (relative changes in timing) shifts in gene expression, relative to amniotes, in the jaw primordia of S. canicula embryos. We demonstrate the presence of clear proximo-distal polarity in gene expression patterns in the shark embryo, thus establishing a baseline molecular baüplan for branchial arch-derived jaw development and further validating the utility of the 'Hinge and Caps' model in comparative studies of jaw development and evolution. Moreover, we correlate gene expression patterns with the absence of a lambdoidal junction (formed where the maxillary first arch meets the frontonasal processes) in chondrichthyans, further highlighting the importance of this region for the development and evolution of jaw structure in advanced gnathostomes.

The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain

“…ScNodal, ScVg1, ScOtx5 and ScFgf8 antisense RNA probes were synthesized from cDNA fragments subcloned in pSPORT1 (ScNodal, ScVg1 and ScFgf8) or pTZ19R (ScOtx5), and sequenced using Universal M13 primers as previously described 31,43,45 . GenBank accession codes for the corresponding sequences are KP698591 for ScNodal, KP698592 for ScVg1, AAK85128.1 for ScOtx5, KP698593 for ScFgf8.…”

Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications

“…Nevertheless, there are no detailed studies about telencephalic tangential routes in basal vertebrates which prevent us from having a comprehensive view of forebrain evolution. The lesser spotted dogfish Scyliorhinus canicula represents a key species in evo-devo studies (Coolen et al 2009;Compagnucci et al 2013). It belongs to the class of Chondrichthyes (chondrichthyans or cartilaginous fishes), an ancient radiation of vertebrates considered the sister group of Teleostomi, i.e., the group of vertebrates with bony skeleton that gave rise to land vertebrates.…”

Neural Crest Cells in Craniofacial Skeletal Development

“…In addition, the lower jaw to upper jaw homeosis observed in Dlx5/6 mutant mice demonstrates the existence of a Hinge-centric patterning program [68]. Recent studies in a chondrichthyan have shown that genes with known polarized jaw expression patterns also have conserved Hinge-(Emx1/2, Nkx3.2) or Cap-centric (Dlx3, Prx1, Msx1, Tbx2, Bmp4) expression patterns (Figure 7.5A) [176]. However, at least some ventralizing signals in the mandible, such as Edn1, seem to be specific to the lower jaw [59,60].…”