Abstract
The origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral (DV) patterning mechanisms within the developing mandibular, hyoid, and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralizing BMP and endothelin signaling pathways and their effectors, the joint markers nkx3.2 and gdf5 and prochondrogenic transcription factor barx1, and the dorsal territory marker pou3f3. Additionally, we find that mesenchymal expression of eya1/six1 is an ancestral feature of the mandibular arch of jawed vertebrates, whereas differences in notch signaling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the DV axis of the pharyngeal arches, including scamp5 as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.
Highlights
The jaw is an iconic example of anatomical innovation, and a uniting feature of the jawed vertebrate crown group (Gans & Northcutt 1983; Mallatt, 1996; Northcutt, 2005)
In mouse (Kurihara et al, 1994; Clouthier et al, 1998; Ozeki et al, 2004) and in zebrafish (Miller et al, 2000; Kimmel et al, 2007), edn1 is expressed in ventral and intermediate mandibular and hyoid arch epithelium, and this edn1 signal is transduced within the adjacent arch mesenchyme through its receptor, ednra, and its downstream effector mef2C (Nair et al, 2007; Miller et al, 2007; Sato et al, 2008). bmp4 is expressed in ventral arch epithelium in mouse (Liu et al, 2005) and in zebrafish (Alexander et al, 2011), where its ventral patterning function is restricted by intermediate expression of grem2, which encodes a secreted Bmp antagonist (Zuniga et al, 2011)
We carried out a series of mRNA in situ hybridisation (ISH) experiments to test for shared expression of ventral patterning factors in the pharyngeal arches of skate embryos
Summary
The jaw is an iconic example of anatomical innovation, and a uniting feature of the jawed vertebrate (gnathostome) crown group (Gans & Northcutt 1983; Mallatt, 1996; Northcutt, 2005). Others, have previously shown that nested expression of the dlx family of transcription factors, a key regulator of DV axial identity in the mandibular arch (Depew et al, 2002, 2005; Beverdam et al, 2002; Talbot et al, 2010), was primitively shared across all pharyngeal arches in gnathostomes (Gillis et al, 2013; Compagnucci et al, 2013; Debiais-Thibaud et al, 2013), and that dorsal and ventral domains of dlx gene expression delineate the principal segments of the jaw and gill arch skeleton in a conserved manner in a chondrichthyan, the skate (Leucoraja erinacea - Gillis et al, 2013) These findings are consistent with hypotheses of serial homology of the palatoquadrate/Meckel’s cartilage and epi-/ceratobranchial gill arch elements, respectively, the degree of conservation or divergence of upstream signals and downstream effectors of this “dlx code” in the mandibular and gill arches has not been fully investigated. Our findings point to a conserved gene regulatory network underlying the primitively shared organisation of the gnathostome mandibular, hyoid and gill arch skeleton, and highlight additional transcriptional features that correlate with the developmental and anatomical diversification of jaws and gill arches within gnathostomes
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