Citation: Erkenbrack, E. M. (2017). Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins. Proceedings of the National Academy of Sciences, 113(46), E7202-E7211.
Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity
To inform the evolution of the echinoderm larval skeletogenic cell, we have presented a framework for cell-type phylogenetic analysis that integrates spatial gene expression data with phylogenetic comparative methods to reconstruct ancestral gene expression. The genes we chose to include in our analyses have been studied in numerous echinoderm taxa and occupy crucial nodes of a well characterized gene regulatory network11,35. As the number of model and nonmodel organisms increases in evolutionary developmental biology, comparative analyses of spatial data will depend more on ancestral state reconstructions than on direct comparisons with an outgroup. However, it should be noted that such analyses are limited by several factors, including knowledge of a detailed GRN, invoking interspecies comparisons of development, and obtaining reliable divergence times and phylogenetic trees. The present study is not exempt from these limitations. Indeed, we chose to analyze five genes with broad phylogenetic sampling over twelve taxa. To support our findings, we ran pruned sensitivity analyses and concluded that decreasing the number of taxa reduced our ability to resolve ancestral states with confidence at certain nodes, especially the Asterozoan and Eleutherozoan MRCAs (Supplementary Fig. 12). Therefore, broad phylogenetic sampling is vitally important to resolve ancestral gene expression patterns. One could argue that increasing the number of genes in the analysis would help resolve the question of interest. However, we suggest that whether or not this is true will depend on the case at hand. For instance, in this study we analyzed genes from a GRN where the functional importance of many regulatory genes is well-known. In most cases, a well characterized GRN will not be available, and it will be equally important to possess a broad sampling of taxa across a phylogeny. For instance, as gene expression in early development becomes available in more asterozoans, which are under-sampled with respect to echinozoans in our analyses, we will gain greater confidence in our inferences at the asterozoan and eleutherozoan MRCAs. Indeed, we also see potential for the approach utilized herein to analyze ancestral states of GRN regulatory architecture. For example, the isolation and characterization of homologous cis-regulatory modules, from ATAC-seq, ChIP-seq, and other omics-level endeavors in phylogenetically distant organisms, could be then incorporated with the method presented here to determine which modules are lineage or cell-type specific.
This work provides direct evidence of evolutionary rewiring of gene-regulatory circuitry accompanying divergence of two subclasses of echinoderm, the cidaroid and euechinoid sea urchins. These forms descend from a known common Paleo- zoic ancestor, and their embryos develop differently, offering an opportunity to probe the basic evolutionary process by which clade divergence occurs at the gene-regulatory net- work (GRN) level. We carried out a systematic analysis of the use of particular genes participating in embryonic skeleto- genic cell specification, building on an established euechinoid developmental GRN. This study revealed that the well-known and elegantly configured regulatory circuitry that underlies skeletogenic specification in modern sea urchins is largely a novel evolutionary invention. The results dramatically dis- play extensive regulatory changes in a specific developmental GRN, underlying an incidence of cladistic divergence at the subclass level.
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