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Gene body methylation evolves during the sustained loss of parental care in the burying beetle

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  • Peter Sarkies

    (University of Oxford)

  • Jennifer Westoby

    (University of Cambridge)

  • Rebecca Mary Kilner

    (University of Cambridge)

  • Rahia Mashoodh

    (University of Cambridge
    University College London)

Abstract

Epigenetic modifications, such as 5-methylcytosine (5mC), can sometimes be transmitted between generations, provoking speculation that epigenetic changes could play a role in adaptation and evolution. Here, we use experimental evolution to investigate how 5mC levels evolve in populations of biparental insect (Nicrophorus vespilloides) derived from a wild source population and maintained independently under different regimes of parental care in the lab. We show that 5mC levels in the transcribed regions of genes (gene bodies) diverge between populations that have been exposed to different levels of care for 30 generations. These changes in 5mC do not reflect changes in the levels of gene expression. However, the accumulation of 5mC within genes between populations is associated with reduced variability in gene expression within populations. Our results suggest that evolved change in 5mC could contribute to phenotypic evolution by influencing variability in gene expression in invertebrates.

Suggested Citation

  • Peter Sarkies & Jennifer Westoby & Rebecca Mary Kilner & Rahia Mashoodh, 2024. "Gene body methylation evolves during the sustained loss of parental care in the burying beetle," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50359-0
    DOI: 10.1038/s41467-024-50359-0
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    References listed on IDEAS

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    1. Samuel V. Arsenault & Brendan G. Hunt & Sandra M. Rehan, 2018. "The effect of maternal care on gene expression and DNA methylation in a subsocial bee," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    2. Claude Becker & Jörg Hagmann & Jonas Müller & Daniel Koenig & Oliver Stegle & Karsten Borgwardt & Detlef Weigel, 2011. "Spontaneous epigenetic variation in the Arabidopsis thaliana methylome," Nature, Nature, vol. 480(7376), pages 245-249, December.
    3. Yi Jin Liew & Emily J. Howells & Xin Wang & Craig T. Michell & John A. Burt & Youssef Idaghdour & Manuel Aranda, 2020. "Intergenerational epigenetic inheritance in reef-building corals," Nature Climate Change, Nature, vol. 10(3), pages 254-259, March.
    4. 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.
    5. Iryna Ivasyk & Leonora Olivos-Cisneros & Stephany Valdés-Rodríguez & Marie Droual & Hosung Jang & Robert J. Schmitz & Daniel J. C. Kronauer, 2023. "DNMT1 mutant ants develop normally but have disrupted oogenesis," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    6. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    7. 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.
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