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Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity

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Abstract

Environmentally acquired microbial symbionts could contribute to host adaptation to local conditions like vertically transmitted symbionts do. This scenario necessitates symbionts to have different effects in different environments. We investigated this idea in Drosophila melanogaster, a species which communities of bacterial symbionts vary greatly among environments. We isolated four bacterial strains isolated from the feces of a D. melanogaster laboratory strain and tested their effects in two conditions: the ancestral environment (i.e. the laboratory medium) and a new environment (i.e. fresh fruit with live yeast). All bacterial effects on larval and adult traits differed among environments, ranging from very beneficial to marginally deleterious. The joint analysis of larval development speed and adult size further shows bacteria affected developmental plasticity more than resource acquisition. This effect was largely driven by the contrasted effects of the bacteria in each environment. Our study illustrates that understanding D. melanogaster symbiotic interactions in the wild will necessitate working in ecologically realistic conditions. Besides, context-dependent effects of symbionts, and their influence on host developmental plasticity, shed light on how environmentally acquired symbionts may contribute to host evolution.

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Acknowledgements

We warmly thank L. Benoit and P. Gautier for methodological help and S. Bourg, M.P. Chapuis, S. Charlat, J. Collet, D. Duneau, O. Duron, R. Gallet, P. Gautier, N. Kremer, F. Leulier, N. Rode and F. Vanlerberghe for useful comments on an earlier version of this work. A previous version of this work is available on bioRxiv (Guilhot et al. 2019) and has been peer-reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100085).

Funding

This project was supported by French National Research Agency through the ‘SWING’ project (ANR-16-CE02-0015) and by Agropolis Fondation under the reference ID 1505-002 through the ‘Investissements d’avenir’ programme (Labex Agro:ANR-10-LABX-0001-01).

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  1. CBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, University of Montpellier, INRAE, Montpellier, France

    Robin Guilhot, Antoine Rombaut, Anne Xuéreb & Simon Fellous

  2. Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, VIC, 3010, Australia

    Kate Howell

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  1. Robin Guilhot
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Correspondence to Robin Guilhot.

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Guilhot, R., Rombaut, A., Xuéreb, A. et al. Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity. Evol Ecol 34, 693–712 (2020). https://doi.org/10.1007/s10682-020-10068-8

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