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Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Author

Listed:
  • Grégoire Vernaz

    (University of Cambridge
    University of Cambridge
    Wellcome Sanger Institute)

  • Milan Malinsky

    (Wellcome Sanger Institute
    University of Bern)

  • Hannes Svardal

    (Wellcome Sanger Institute
    University of Antwerp
    Naturalis Biodiversity Center)

  • Mingliu Du

    (University of Cambridge
    University of Cambridge
    Wellcome Sanger Institute)

  • Alexandra M. Tyers

    (Sciences, Bangor University
    Max Planck Institute for Biology of Ageing)

  • M. Emília Santos

    (University of Cambridge)

  • Richard Durbin

    (University of Cambridge
    Wellcome Sanger Institute)

  • Martin J. Genner

    (University of Bristol)

  • George F. Turner

    (Sciences, Bangor University)

  • Eric A. Miska

    (University of Cambridge
    University of Cambridge
    Wellcome Sanger Institute)

Abstract

Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

Suggested Citation

  • Grégoire Vernaz & Milan Malinsky & Hannes Svardal & Mingliu Du & Alexandra M. Tyers & M. Emília Santos & Richard Durbin & Martin J. Genner & George F. Turner & Eric A. Miska, 2021. "Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26166-2
    DOI: 10.1038/s41467-021-26166-2
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    References listed on IDEAS

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    1. David Brawand & Catherine E. Wagner & Yang I. Li & Milan Malinsky & Irene Keller & Shaohua Fan & Oleg Simakov & Alvin Y. Ng & Zhi Wei Lim & Etienne Bezault & Jason Turner-Maier & Jeremy Johnson & Rosa, 2014. "The genomic substrate for adaptive radiation in African cichlid fish," Nature, Nature, vol. 513(7518), pages 375-381, September.
    2. Matthew D. McGee & Samuel R. Borstein & Joana I. Meier & David A. Marques & Salome Mwaiko & Anthony Taabu & Mary A. Kishe & Brian O’Meara & Rémy Bruggmann & Laurent Excoffier & Ole Seehausen, 2020. "The ecological and genomic basis of explosive adaptive radiation," Nature, Nature, vol. 586(7827), pages 75-79, October.
    3. Catherine S. Lee & Joshua R. Friedman & James T. Fulmer & Klaus H. Kaestner, 2005. "The initiation of liver development is dependent on Foxa transcription factors," Nature, Nature, vol. 435(7044), pages 944-947, June.
    4. M. Emília Santos & Ingo Braasch & Nicolas Boileau & Britta S. Meyer & Loïc Sauteur & Astrid Böhne & Heinz-Georg Belting & Markus Affolter & Walter Salzburger, 2014. "The evolution of cichlid fish egg-spots is linked with a cis-regulatory change," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    5. Pilar Cubas & Coral Vincent & Enrico Coen, 1999. "An epigenetic mutation responsible for natural variation in floral symmetry," Nature, Nature, vol. 401(6749), pages 157-161, September.
    6. Nicola J. Nadeau & Carolina Pardo-Diaz & Annabel Whibley & Megan A. Supple & Suzanne V. Saenko & Richard W. R. Wallbank & Grace C. Wu & Luana Maroja & Laura Ferguson & Joseph J. Hanly & Heather Hines , 2016. "The gene cortex controls mimicry and crypsis in butterflies and moths," Nature, Nature, vol. 534(7605), pages 106-110, June.
    7. Taewoo Ryu & Heather D. Veilleux & Jennifer M. Donelson & Philip L. Munday & Timothy Ravasi, 2018. "The epigenetic landscape of transgenerational acclimation to ocean warming," Nature Climate Change, Nature, vol. 8(6), pages 504-509, June.
    8. Robert E. Thurman & Eric Rynes & Richard Humbert & Jeff Vierstra & Matthew T. Maurano & Eric Haugen & Nathan C. Sheffield & Andrew B. Stergachis & Hao Wang & Benjamin Vernot & Kavita Garg & Sam John &, 2012. "The accessible chromatin landscape of the human genome," Nature, Nature, vol. 489(7414), pages 75-82, September.
    9. Giacomo Cavalli & Edith Heard, 2019. "Advances in epigenetics link genetics to the environment and disease," Nature, Nature, vol. 571(7766), pages 489-499, July.
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