• Share

Juvenile skeletogenesis in anciently diverged sea urchin clades
Citation: Gao, F., Thompson, J. R., Petsios, E., Erkenbrack, E., Moats, R. A., Bottjer, D. J., & Davidson, E. H. (2015). Juvenile skeletogenesis in anciently diverged sea urchin clades. Developmental biology, 400(1), 148-158.
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.

More Publications

The mammalian decidual cell evolved from a cellular stress response

Animals consist of a wide variety of cells that serve different functions depending on their location in the body. Cells with similar functions, or cell types, in different animal species are related both by an evolutionary line of descentÐsimilar to the relatedness of species themselvesÐand by a developmental line of descent in the embryo. Networks of interacting genes, or gene regulatory networks, control gene expression in the cell, thereby specifying cell type identity. Understanding how new cell types arise by changing gene regulatory networks is critical both to comprehending fundamental aspects of human biology and to manipulating cell types in the laboratory. We approached this question by studying endometrial stromal fibroblast (ESF) cells from the uterus of humans and opossums, two distantly related mammals. We showed that the distantly related cell type in opossum expresses a similar set of regulatory genes as the human cell, but in response to pregnancy-related signals, the opossum cells induce a stress response. In the human cells, these signals induce differentiation into decidual cells, a specialized cell type present in humans and closely related mammals. These results suggest that a gene regulatory network that modulated an ancestral, pregnancy-related stress response was hijacked and repurposed to function in differentiation and specification of the decidual cell type.

A Conserved Role for VEGF Signaling in Specification of Homologous Mesenchymal Cell Types Positioned at Spatially Distinct Developmental Addresses in Early Development of Sea Urchins

Comparative studies of early development in echinoderms are revealing the tempo and mode of alterations to developmental gene regulatory networks and to the cell types they specify. In euechinoid sea urchins, skeletogenic mesenchyme (SM) ingresses prior to gastrulation at the vegetal pole and aligns into a ring-like array with two bilateral pockets of cells, the sites where spiculogenesis will later occur. In cidaroid sea urchins, the anciently diverged sister clade to euechinoid sea urchins, a homologous SM cell type ingresses later in development, after gastrulation has commenced, and consequently at a distinct developmental address. Thus, a heterochronic shift of ingression of the SM cell type occurred in one of the echinoid lineages. In euechinoids, speci cation and migration of SM are facilitated by vascular endothelial growth factor (VEGF) signaling. We describe spatiotemporal expression of vegf and vegfr and experimental manipulations target- ing VEGF signaling in the cidaroid Eucidaris tribuloides.
© 2016 Eric M Erkenbrack and Elsevier. All rights reserved.