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Maternal transmission as a microbial symbiont sieve, and the absence of lactation in male mammals

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  • Brennen T. Fagan

    (University of York
    University of York)

  • George W. A. Constable

    (University of York)

  • Richard Law

    (University of York)

Abstract

Gut microbiomes of mammals carry a complex symbiotic assemblage of microorganisms. Feeding newborn infants milk from the mammary gland allows vertical transmission of the parental milk microbiome to the offspring’s gut microbiome. This has benefits, but also has hazards for the host population. Using mathematical models, we demonstrate that biparental vertical transmission enables deleterious microbial elements to invade host populations. In contrast, uniparental vertical transmission acts as a sieve, preventing these invasions. Moreover, we show that deleterious symbionts generate selection on host modifier genes that keep uniparental transmission in place. Since microbial transmission occurs during birth in placental mammals, subsequent transmission of the milk microbiome needs to be maternal to avoid the spread of deleterious elements. This paper therefore argues that viviparity and the hazards from biparental transmission of the milk microbiome, together generate selection against male lactation in placental mammals.

Suggested Citation

  • Brennen T. Fagan & George W. A. Constable & Richard Law, 2024. "Maternal transmission as a microbial symbiont sieve, and the absence of lactation in male mammals," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49559-5
    DOI: 10.1038/s41467-024-49559-5
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    1. Helen M Kurkjian & M Javad Akbari & Babak Momeni, 2021. "The impact of interactions on invasion and colonization resistance in microbial communities," PLOS Computational Biology, Public Library of Science, vol. 17(1), pages 1-18, January.
    2. Marcus C. de Goffau & Susanne Lager & Ulla Sovio & Francesca Gaccioli & Emma Cook & Sharon J. Peacock & Julian Parkhill & D. Stephen Charnock-Jones & Gordon C. S. Smith, 2019. "Human placenta has no microbiome but can contain potential pathogens," Nature, Nature, vol. 572(7769), pages 329-334, August.
    3. Akshit Goyal & Tong Wang & Veronika Dubinkina & Sergei Maslov, 2021. "Ecology-guided prediction of cross-feeding interactions in the human gut microbiome," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Jesús Manuel García-Acosta & Rosa María San Juan-Valdivia & Alfredo David Fernández-Martínez & Nieves Doria Lorenzo-Rocha & Maria Elisa Castro-Peraza, 2019. "Trans* Pregnancy and Lactation: A Literature Review from a Nursing Perspective," IJERPH, MDPI, vol. 17(1), pages 1-12, December.
    5. Christopher J. Stewart & Nadim J. Ajami & Jacqueline L. O’Brien & Diane S. Hutchinson & Daniel P. Smith & Matthew C. Wong & Matthew C. Ross & Richard E. Lloyd & HarshaVardhan Doddapaneni & Ginger A. M, 2018. "Temporal development of the gut microbiome in early childhood from the TEDDY study," Nature, Nature, vol. 562(7728), pages 583-588, October.
    6. Marcus C. Goffau & Susanne Lager & Ulla Sovio & Francesca Gaccioli & Emma Cook & Sharon J. Peacock & Julian Parkhill & D. Stephen Charnock-Jones & Gordon C. S. Smith, 2019. "Author Correction: Human placenta has no microbiome but can contain potential pathogens," Nature, Nature, vol. 574(7778), pages 15-15, October.
    7. Kevin R. Foster & Jonas Schluter & Katharine Z. Coyte & Seth Rakoff-Nahoum, 2017. "The evolution of the host microbiome as an ecosystem on a leash," Nature, Nature, vol. 548(7665), pages 43-51, August.
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