Dev Biol 2015 Apr 01;4001:148-58. doi: 10.1016/j.ydbio.2015.01.017.

Juvenile skeletogenesis in anciently diverged sea urchin clades.

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Mechanistic understanding of evolutionary divergence in animal body plans devolves from analysis of those developmental processes that, in forms descendant from a common ancestor, are responsible for their morphological differences. The last common ancestor of the two extant subclasses of sea urchins, i.e., euechinoids and cidaroids, existed well before the Permian/Triassic extinction (252 mya). Subsequent evolutionary divergence of these clades offers in principle a rare opportunity to solve the developmental regulatory events underlying a defined evolutionary divergence process. Thus (i) there is an excellent and fairly dense (if yet incompletely analyzed) fossil record; (ii) cladistically confined features of the skeletal structures of modern euechinoid and cidaroid sea urchins are preserved in fossils of ancestral forms; (iii) euechinoids and cidaroids are among current laboratory model systems in molecular developmental biology (here Strongylocentrotus purpuratus [Sp] and Eucidaris tribuloides [Et]); (iv) skeletogenic specification in sea urchins is uncommonly well understood at the causal level of interactions of regulatory genes with one another, and with known skeletogenic effector genes, providing a ready arsenal of available molecular tools. Here we focus on differences in test and perignathic girdle skeletal morphology that distinguish all modern euechinoid from all modern cidaroid sea urchins. We demonstrate distinct canonical test and girdle morphologies in juveniles of both species by use of SEM and X-ray microtomography. Among the sharply distinct morphological features of these clades are the internal skeletal structures of the perignathic girdle to which attach homologous muscles utilized for retraction and protraction of Aristotles׳ lantern and its teeth. We demonstrate that these structures develop de novo between one and four weeks after metamorphosis. In order to study the underlying developmental processes, a method of section whole mount in situ hybridization was adapted. This method displays current gene expression in the developing test and perignathic girdle skeletal elements of both Sp and Et juveniles. Active, specific expression of the sm37 biomineralization gene in these muscle attachment structures accompanies morphogenetic development of these clade-specific features in juveniles of both species. Skeletogenesis at these clade-specific muscle attachment structures displays molecular earmarks of the well understood embryonic skeletogenic GRN: thus the upstream regulatory gene alx1 and the gene encoding the vegfR signaling receptor are both expressed at the sites where they are formed. This work opens the way to analysis of the alternative spatial specification processes that were installed at the evolutionary divergence of the two extant subclasses of sea urchins.

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Genes referenced: alx1 LOC100887844 LOC575170