During growth, individual skull bones overlap at sutures, where osteoblast differentiation and bone deposition occur. Mutations causing skull malformations have revealed some required genes, but many aspects of suture regulation remain poorly understood. We describe a zebrafish mutation in osterix/sp7, which causes a generalized delay in osteoblast maturation. While most of the skeleton is patterned normally, mutants have specific defects in the anterior skull and upper jaw, and the top of the skull comprises a random mosaic of bones derived from individual initiation sites. Osteoblasts at the edges of the bones are highly proliferative and fail to differentiate, consistent with global changes in gene expression. We propose that signals from the bone itself are required for orderly recruitment of precursor cells and growth along the edges. The delay in bone maturation caused by loss of Sp7 leads to unregulated bone formation, revealing a new mechanism for patterning the skull and sutures.

BackgroundA major goal of evolutionary biology is to understand the origins of phenotypic diversity. Changes in development, for instance heterochrony, can be a potent source of phenotypic variation. On the other hand, development can also constrain the spectrum of phenotypes that can be produced. In order to understand these dual roles of development in evolution, we examined the developmental trajectory of a trait central to the extensive adaptive radiation of East African cichlid fishes: craniofacial adaptations that allow optimal exploitation of ecological niches. Specifically, we use geometric morphometric analysis to compare morphological ontogenies among six species of Lake Malawi cichlids (n > 500 individuals) that span a major ecomorphological axis. We further evaluate how modulation of Wnt signaling impacts the long-term developmental trajectory of facial development.ResultsWe find that, despite drastic differences in adult craniofacial morphologies, there are general similarities in the path of craniofacial ontogeny among species, suggesting that natural selection is working within a conserved developmental program. However, we also detect species-specific differences in the timing, direction, and/or duration of particular developmental trajectories, including evidence of heterochrony. Previous work in cichlids and other systems suggests that species-specific differences in adult morphology are due to changes in molecular signaling pathways that regulate early craniofacial development. In support of this, we demonstrate that modulation of Wnt signaling at early stages can shift a developmental trajectory into morphospace normally occupied by another species. However, without sustained modulation, craniofacial shape can recover by juvenile stages. This underscores the idea that craniofacial development is robust and that adult head shapes are the product of many molecular changes acting over extended periods of development.ConclusionsOur results are consistent with the hypothesis that development acts to both constrain and promote morphological diversity. They also illustrate the modular nature of the craniofacial skeleton and hence the ability of selection to act upon distinct anatomical features in an independent manner. We propose that trophic diversity among cichlids has been achieved via shifts in both specific (e.g., stage-specific changes in gene expression) and global (e.g., heterochrony) ontogenetic processes acting within a conserved developmental program.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0020-8) contains supplementary material, which is available to authorized users.