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

Publication ,  Journal Article
Davidson, PL; Guo, H; Swart, JS; Massri, AJ; Edgar, A; Wang, L; Berrio, A; Devens, HR; Koop, D; Cisternas, P; Zhang, H; Zhang, Y; Byrne, M ...
Published in: Nature ecology & evolution
December 2022

Changes in developmental gene regulatory networks (dGRNs) underlie much of the diversity of life, but the evolutionary mechanisms that operate on regulatory interactions remain poorly understood. Closely related species with extreme phenotypic divergence provide a valuable window into the genetic and molecular basis for changes in dGRNs and their relationship to adaptive changes in organismal traits. Here we analyse genomes, epigenomes and transcriptomes during early development in two Heliocidaris sea urchin species that exhibit highly divergent life histories and in an outgroup species. Positive selection and chromatin accessibility modifications within putative regulatory elements are enriched on the branch leading to the derived life history, particularly near dGRN genes. Single-cell transcriptomes reveal a dramatic delay in cell fate specification in the derived state, which also has far fewer open chromatin regions, especially near conserved cell fate specification genes. Experimentally perturbing key transcription factors reveals profound evolutionary changes to early embryonic patterning events, disrupting regulatory interactions previously conserved for ~225 million years. These results demonstrate that natural selection can rapidly reshape developmental gene expression on a broad scale when selective regimes abruptly change. More broadly, even highly conserved dGRNs and patterning mechanisms in the early embryo remain evolvable under appropriate ecological circumstances.

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Published In

Nature ecology & evolution

DOI

EISSN

2397-334X

ISSN

2397-334X

Publication Date

December 2022

Volume

6

Issue

12

Start / End Page

1907 / 1920

Related Subject Headings

  • Sea Urchins
  • Gene Regulatory Networks
  • Chromatin
  • Biological Evolution
  • Anthocidaris
  • Animals
  • 4104 Environmental management
  • 3104 Evolutionary biology
  • 3103 Ecology
 

Citation

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Davidson, P. L., Guo, H., Swart, J. S., Massri, A. J., Edgar, A., Wang, L., … Wray, G. A. (2022). Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins. Nature Ecology & Evolution, 6(12), 1907–1920. https://doi.org/10.1038/s41559-022-01906-9
Davidson, Phillip L., Haobing Guo, Jane S. Swart, Abdull J. Massri, Allison Edgar, Lingyu Wang, Alejandro Berrio, et al. “Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins.Nature Ecology & Evolution 6, no. 12 (December 2022): 1907–20. https://doi.org/10.1038/s41559-022-01906-9.
Davidson PL, Guo H, Swart JS, Massri AJ, Edgar A, Wang L, et al. Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins. Nature ecology & evolution. 2022 Dec;6(12):1907–20.
Davidson, Phillip L., et al. “Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins.Nature Ecology & Evolution, vol. 6, no. 12, Dec. 2022, pp. 1907–20. Epmc, doi:10.1038/s41559-022-01906-9.
Davidson PL, Guo H, Swart JS, Massri AJ, Edgar A, Wang L, Berrio A, Devens HR, Koop D, Cisternas P, Zhang H, Zhang Y, Byrne M, Fan G, Wray GA. Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins. Nature ecology & evolution. 2022 Dec;6(12):1907–1920.

Published In

Nature ecology & evolution

DOI

EISSN

2397-334X

ISSN

2397-334X

Publication Date

December 2022

Volume

6

Issue

12

Start / End Page

1907 / 1920

Related Subject Headings

  • Sea Urchins
  • Gene Regulatory Networks
  • Chromatin
  • Biological Evolution
  • Anthocidaris
  • Animals
  • 4104 Environmental management
  • 3104 Evolutionary biology
  • 3103 Ecology