Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins

Abstract

Chromatin configuration is highly dynamic during embryonic development in animals, exerting an important point of control in transcriptional regulation. Yet there exists remarkably little information about the contribution of evolutionary changes in chromatin configuration to the evolution of gene expression and organismal traits. Genome-wide assays of chromatin configuration, coupled with whole-genome alignments, can help address this gap in knowledge in several ways. In this study we present a comparative analysis of regulatory element sequences and accessibility throughout embryogenesis in three sea urchin species with divergent life histories: a lecithotroph Heliocidaris erythrogramma, a closely related planktotroph H. tuberculata, and a distantly related planktotroph Lytechinus variegatus. We identified distinct epigenetic and mutational signatures of evolutionary modifications to cis-regulatory element function in H. erythrogramma that have accumulated non-uniformly throughout the genome, suggesting selection, rather than drift, underlies many modifications associated with the derived life history. Specifically, regulatory elements composing the sea urchin developmental gene regulatory network are enriched for signatures of positive selection and accessibility changes which may function to alter binding affinity and access of developmental transcription factors to these sites. Furthermore, regulatory element changes often correlate with divergent expression patterns of genes involved in cell type specification, morphogenesis, and development of other derived traits, suggesting these evolutionary modifications have been consequential for phenotypic evolution in H. erythrogramma. Collectively, our results demonstrate that selective pressures imposed by changes in developmental life history rapidly reshape the cis-regulatory landscape of core developmental genes to generate novel traits and embryonic programs.

Hybrid epigenomes reveal extensive local genetic changes to chromatin accessibility contribute to divergence in embryonic gene expression between species

“…This result is consistent with many other studies that find core promoter regions to be generally more open than distal enhancers (Klemm, et al 2019). Peaks in hybrids corresponding to putative promoter regions and enhancer regions are similar in size to those in same-species crosses (Davidson, et al 2022), suggesting that biological effects outweigh technical influences on read mapping in hybrids.…”

“…Indeed, the number of DA OCRs with maternal dominance is lowest in absolute terms at the earliest stage (blastula) and nearly doubles by the gastrula stage (15,580 to 27,381). Although it may seem paradoxical for maternal effects to increase over developmental time, this is made possible by the fact that more and more OCRs become accessible during development (Davidson, et al 2022),resulting in the relative proportion of maternal dominant peaks remaining roughly stable over time despite an increase in their absolute number . These observations suggest that maternal effects on the chromatin landscape persist much longer during development than do maternal effects on transcript abundance, and are notably more extensive at later stages.…”

“…Transcriptional states in sea urchin embryos are driven by a well-defined gene regulatory network Saudemont, et al 2010;Erkenbrack, et al 2018). Previous work has established that 1) the genetic mechanisms governing the regulation of these genes differ from those controlling gene expression as a whole (Wang, et al 2020), and 2) putative regulatory elements near these genes are under greater selective pressure than the rest of the epigenomic landscape (Davidson, et al 2022).Thus, we also examined how the open chromatin landscape near GRN genes compared to the epigenome as a whole. We found that the density distribution of peaks near (within 25 kb) of a GRN gene was significantly different from the density distribution of peaks in the entire genome (Scheffe test and Kolmogorov-Smirnov test), with GRN genes having more nearby peaks than non-GRN genes.…”

“…From a mechanistic perspective, opening chromatin is permissive rather than determinative: unless the appropriate transcription factors are present, a change in accessibility alone will not alter transcription. This is clearly illustrated by the observation that many OCRs open prior to the onset of transcription of any nearby gene during development, including in sea urchins specifically (Shashikant, et al 2018b;Davidson, et al 2022).…”

Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins

“…Fig.2b: hesC ). Because decreased chromatin accessibility can limit transcription factor access to regulatory elements and because most regulatory interactions in the early sea urchin embryo involve activation of transcription 24 , widespread evolutionary reduction in chromatin accessibility throughout the genome in H. erythrogramma embryos suggests an important role for evolutionary changes in chromatin configuration for divergence in gene expression, in this case associated with generally decreased or delayed zygotic transcription for many genes. This interpretation is consistent with indications of a broad delay in embryonic cell fate specification in this species 19,25-29 .…”