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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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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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.
Because marine sponges are invertebrates, no permission was sought or required in order to conduct field sampling.
The authors declare no competing interests.
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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