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Vertical transmission of sponge microbiota is inconsistent and unfaithful

Nature Ecology & Evolution volume 3, pages 1172–1183 (2019)Cite this article

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An Author Correction to this article was published on 02 March 2021

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Abstract

Co-evolutionary theory predicts that if beneficial microbial symbionts improve host fitness, they should be faithfully transmitted to offspring. More recently, the hologenome theory of evolution predicts resemblance between parent and offspring microbiomes and high partner fidelity between host species and their vertically transmitted microbes. Here, we test these ideas in multiple coexisting host species with highly diverse microbiota, leveraging known parent–offspring pairs sampled from eight species of wild marine sponges (Porifera). We found that the processes governing vertical transmission were both neutral and selective. A neutral model was a better fit to larval (R 2 = 0.66) than to the adult microbiota (R 2 = 0.27), suggesting that the importance of non-neutral processes increases as the sponge host matures. Microbes that are enriched above neutral expectations in adults were disproportionately transferred to offspring. Patterns of vertical transmission were, however, incomplete: larval sponges shared, on average, 44.8% of microbes with their parents, which was not higher than the fraction they shared with nearby non-parental adults. Vertical transmission was also inconsistent across siblings, as larval sponges from the same parent shared only 17% of microbes. Finally, we found no evidence that vertically transmitted microbes are faithful to a single sponge host species. Surprisingly, larvae were as likely to share vertically transmitted microbes with larvae from other sponge species as they were with their own species. Our study demonstrates that common predictions of vertical transmission that stem from species-poor systems are not necessarily true when scaling up to diverse and complex microbiomes.

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Fig. 1: Taxonomic diversity is distributed along a sponge-specific axis.
Fig. 2: The processes underlying symbiont acquisition are both neutral and selective.
Fig. 3: Taxa that are enriched above neutral expectations in adults are disproportionately transferred to offspring.
Fig. 4: Taxonomic profiles of the microbiota between parents and offspring.
Fig. 5: Offspring does not share more taxa with its parent than with other conspecific adults, but siblings receive a small set of identical symbionts from their parent.
Fig. 6: Conspecific adults and larvae do not share more vertically transmitted taxa than heterospecific hosts.

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Data availability

All sequence data are part of the Sponge EMP and can be downloaded from https://github.com/amnona/SpongeEMP. Data and code used in the focal study can be downloaded from https://osf.io/jg69k/. The raw sequences analysed in this study can be extracted from the Sponge EMP data using the accession numbers available in the focal metadata.

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Acknowledgements

We thank R. Coma and E. Serrano for help with sponge taxonomic identification, and E. Canals Sallent and E. Serrano for help with field sampling. J.R.B. was supported by an FPI Fellowship from the Spanish Government (No. BES-2011-049043). J.M.M. was supported by the French LabEx TULIP (Nos. ANR-10-LABX-41 and ANR-11-IDEX-002-02), by the Region Midi-Pyrenees project (No. CNRS 121090) and by the FRAGCLIM Consolidator Grant, funded by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 726176). This project also received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 796011.

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  1. These authors jointly supervised this work: Elizabeth A. Archie and José M. Montoya.

Authors and Affiliations

  1. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA

    Johannes R. Björk & Elizabeth A. Archie

  2. Theoretical and Experimental Ecology Station, CNRS-University Paul Sabatier, Moulis, France

    Johannes R. Björk & José M. Montoya

  3. Natural History Museum, London, UK

    Cristina Díez-Vives

  4. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Carmen Astudillo-García

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Contributions

J.R.B. and J.M.M. conceived the study. J.R.B. performed the fieldwork and analysed the data. J.R.B. and J.M.M. drafted the first versions of the manuscript. J.R.B. and E.A. refined the ideas and wrote the final version of the paper. C.D. helped in the field and extracted DNA from the larvae. C.A.G. identified the sponge-specific clusters. All authors commented on and approved of later versions of the paper.

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Correspondence to Johannes R. Björk, Elizabeth A. Archie or José M. Montoya.

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Björk, J.R., Díez-Vives, C., Astudillo-García, C. et al. Vertical transmission of sponge microbiota is inconsistent and unfaithful. Nat Ecol Evol 3, 1172–1183 (2019). https://doi.org/10.1038/s41559-019-0935-x

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