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Microbiome and epigenetic variation in wild fish with low genetic diversity

Author

Listed:
  • Ishrat Z. Anka

    (Swansea University
    Chattogram Veterinary and Animal Sciences University)

  • Tamsyn M. Uren Webster

    (Swansea University)

  • Waldir M. Berbel-Filho

    (University of Oklahoma
    University of West Florida)

  • Matthew Hitchings

    (Swansea University)

  • Benjamin Overland

    (Swansea University)

  • Sarah Weller

    (Swansea University)

  • Carlos Garcia de Leaniz

    (Swansea University
    Universidade de Vigo)

  • Sofia Consuegra

    (Swansea University
    Instituto de Investigacións Mariñas)

Abstract

Non-genetic sources of phenotypic variation, such as the epigenome and the microbiome, could be important contributors to adaptive variation for species with low genetic diversity. However, little is known about the complex interaction between these factors and the genetic diversity of the host, particularly in wild populations. Here, we examine the skin microbiome composition of two closely-related mangrove killifish species with different mating systems (self-fertilising and outcrossing) under sympatric and allopatric conditions. This allows us to partition the influence of the genotype and the environment on their microbiome and (previously described) epigenetic profiles. We find the diversity and community composition of the skin microbiome are strongly shaped by the environment and, to a lesser extent, by species-specific influences. Heterozygosity and microbiome alpha diversity, but not epigenetic variation, are associated with the fluctuating asymmetry of traits related to performance (vision) and behaviour (aggression). Our study identifies that a proportion of the epigenetic diversity and microbiome differentiation is unrelated to genetic variation, and we find evidence for an associative relationship between microbiome and epigenetic diversity in these wild populations. This suggests that both mechanisms could potentially contribute to variation in species with low genetic diversity.

Suggested Citation

  • Ishrat Z. Anka & Tamsyn M. Uren Webster & Waldir M. Berbel-Filho & Matthew Hitchings & Benjamin Overland & Sarah Weller & Carlos Garcia de Leaniz & Sofia Consuegra, 2024. "Microbiome and epigenetic variation in wild fish with low genetic diversity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49162-8
    DOI: 10.1038/s41467-024-49162-8
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    References listed on IDEAS

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    1. Laura Baldassarre & Hua Ying & Adam M. Reitzel & Sören Franzenburg & Sebastian Fraune, 2022. "Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Goslee, Sarah C. & Urban, Dean L., 2007. "The ecodist Package for Dissimilarity-based Analysis of Ecological Data," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 22(i07).
    3. Lucas P. Henry & Marjolein Bruijning & Simon K. G. Forsberg & Julien F. Ayroles, 2021. "The microbiome extends host evolutionary potential," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
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