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

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 role
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 the function of putative cis-regulatory
elements 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.