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Parallel and convergent genomic changes underlie independent subterranean colonization across beetles

Author

Listed:
  • Pau Balart-García

    (Institute of Evolutionary Biology (CSIC - Universitat Pompeu Fabra))

  • Leandro Aristide

    (Institute of Evolutionary Biology (CSIC - Universitat Pompeu Fabra))

  • Tessa M. Bradford

    (University of Adelaide
    South Australian Museum)

  • Perry G. Beasley-Hall

    (University of Adelaide
    South Australian Museum)

  • Slavko Polak

    (Notranjska Museum Postojna)

  • Steven J. B. Cooper

    (University of Adelaide
    South Australian Museum)

  • Rosa Fernández

    (Institute of Evolutionary Biology (CSIC - Universitat Pompeu Fabra))

Abstract

Adaptation to life in caves is often accompanied by dramatically convergent changes across distantly related taxa, epitomized by the loss or reduction of eyes and pigmentation. Nevertheless, the genomic underpinnings underlying cave-related phenotypes are largely unexplored from a macroevolutionary perspective. Here we investigate genome-wide gene evolutionary dynamics in three distantly related beetle tribes with at least six instances of independent colonization of subterranean habitats, inhabiting both aquatic and terrestrial underground systems. Our results indicate that remarkable gene repertoire changes mainly driven by gene family expansions occurred prior to underground colonization in the three tribes, suggesting that genomic exaptation may have facilitated a strict subterranean lifestyle parallelly across beetle lineages. The three tribes experienced both parallel and convergent changes in the evolutionary dynamics of their gene repertoires. These findings pave the way towards a deeper understanding of the evolution of the genomic toolkit in hypogean fauna.

Suggested Citation

  • Pau Balart-García & Leandro Aristide & Tessa M. Bradford & Perry G. Beasley-Hall & Slavko Polak & Steven J. B. Cooper & Rosa Fernández, 2023. "Parallel and convergent genomic changes underlie independent subterranean colonization across beetles," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39603-1
    DOI: 10.1038/s41467-023-39603-1
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    References listed on IDEAS

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    1. Fran Supek & Matko Bošnjak & Nives Škunca & Tomislav Šmuc, 2011. "REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms," PLOS ONE, Public Library of Science, vol. 6(7), pages 1-9, July.
    2. Andrew C. Elden & Hyung-Jun Kim & Michael P. Hart & Alice S. Chen-Plotkin & Brian S. Johnson & Xiaodong Fang & Maria Armakola & Felix Geser & Robert Greene & Min Min Lu & Arun Padmanabhan & Dana Clay-, 2010. "Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS," Nature, Nature, vol. 466(7310), pages 1069-1075, August.
    3. Boaz Cook & Robert W. Hardy & William B. McConnaughey & Charles S. Zuker, 2008. "Preserving cell shape under environmental stress," Nature, Nature, vol. 452(7185), pages 361-364, March.
    4. Wesley C. Warren & Tyler E. Boggs & Richard Borowsky & Brian M. Carlson & Estephany Ferrufino & Joshua B. Gross & LaDeana Hillier & Zhilian Hu & Alex C. Keene & Alexander Kenzior & Johanna E. Kowalko , 2021. "A chromosome-level genome of Astyanax mexicanus surface fish for comparing population-specific genetic differences contributing to trait evolution," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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