Abstract
The vertebrate jaw is a versatile feeding apparatus that facilitated explosive diversification. Its functions require a joint between the upper and lower jaws, so jaw joint defects — such as osteoarthritis or even ankylosis — are often highly disruptive and difficult to study. To describe consequences of jaw joint dysfunction, we engineered two independent null alleles of a single jaw-joint marker gene, nkx3.2, in zebrafish. The mutations caused the fish to become functionally jawless via a fusion between the upper and lower jaw cartilages (ankylosis). Surviving to adulthood despite lacking jaw joints, nkx3.2 mutants accommodate this defect by: a) remodeling their skulls drastically from juvenile to adult stages; and b) altering their feeding behaviors from suction to ram feeding. As a result of the remodeling, nkx3.2 mutants developed superficial similarities to the skull shapes observed in two lineages of ancient jawless vertebrates (anaspids and furcacaudiform thelodonts), including: a fixed open gape, reduced snout, and enlarged branchial region. However, no homology exists in individual skull elements between these taxa, and most of the modified elements in the mutant zebrafish occur outside known expression domains of nkx3.2. Therefore, we interpret the adult nkx3.2 phenotype not as a reversal to an ancestral state, but as convergence due to similar functional requirement of feeding without mobile jaws. This remarkable convergence underscores jaw joint functions as a powerful constraint during the development of jawed vertebrate skulls, which implies that functionally viable morphological patterns are finite, with or without functional jaws. Because nkx3.2 null zebrafish display prominent joint ankylosis, drastically modified skull shape, and altered feeding behaviors, these mutants provide a unique model with which to investigate mechanisms of skeletal remodeling and joint diseases.