Abstract

The multiplicity of cell types comprising multicellular organisms begs the question as to how cell type identities evolve over time. Cell type phylogenetics informs this question by comparing gene expression of homologous cell types in distantly related taxa. We employ this approach to inform the identity of larval skeletogenic cells of echinoderms, a clade for which there are phylogenetically diverse datasets of spatial gene expression patterns. We determined ancestral spatial expression patterns of alx1, ets1, tbr, erg, and vegfr, key components of the skeletogenic gene regulatory network driving identity of the larval skeletogenic cell. Here we show ancestral state reconstructions of spatial gene expression of extant eleutherozoan echinoderms support homology and common ancestry of echinoderm larval skeletogenic cells. We propose larval skeletogenic cells arose in the stem lineage of eleutherozoans during a cell type duplication event that heterochronically activated adult skeletogenic cells in a topographically distinct tissue in early development.

Highlights

  • The multiplicity of cell types comprising multicellular organisms begs the question as to how cell type identities evolve over time

  • We assembled a database of spatial gene-expression data for similar timepoints in early development for alx[1], erg, ets[1], tbrain, and vegfr, regulatory genes that underlie specification of these cells based on the published gene regulatory networks (GRNs) at http://echinobase.org/endomes/, and scored spatial distribution of their expression as character states (Fig. 1 and Supplementary Data 1)

  • 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

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Summary

Introduction

The multiplicity of cell types comprising multicellular organisms begs the question as to how cell type identities evolve over time. We frame spatial gene expression data of regulatory genes driving euechinoid larval skeletogenic cell identity from numerous echinoderms in the context of cell type evolution to inform the relatedness of echinoderm larval skeletogenic cells. Our analyses are consistent with the hypothesis that larval skeletogenic cells arose once in the stem lineage of eleutherozoan echinoderms We propose that this event was a cell-type duplication event involving activation of the adult skeletogenic cell during early development. This evolutionary event gave rise to a sister cell type, the larval skeletogenic cell, that was subsequently individuated or lost in different lineages of extant eleutherozoans. Our analysis affords a method to rigorously determine ancestral states of spatial gene expression patterns, thereby revealing how cell-type identity changes over vast expanses of evolutionary time

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