Environmental specificity in Drosophila -bacteria symbiosis affects host developmental plasticity

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Environmental specificity in Drosophila‑bacteria symbiosis affects host developmental plasticity Robin Guilhot1   · Antoine Rombaut1 · Anne Xuéreb1 · Kate Howell2 · Simon Fellous1 Received: 1 July 2020 / Accepted: 17 August 2020 © Springer Nature Switzerland AG 2020

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. Keywords  Symbiosis · Extracellular bacteria · Drosophila melanogaster · Life history traits · Developmental plasticity · Resource acquisition

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1068​ 2-020-10068​-8) contains supplementary material, which is available to authorized users. * Robin Guilhot [email protected] 1

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

2

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



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Evolutionary Ecology

Introduction Symbiosis may contribute to host evolution through recruitment of beneficial microorganisms (Margulis and Fester 1991; Jaenike et al. 2010; Fellous et al. 2011). As the environment varies among localities, different symbionts may be most beneficial in different conditions (De Vries et  al. 2004; Daskin and Alford 2012; Bresson et  al. 2013; Cass et  al. 2016; Couret et  al. 2019), possibly explaining microbiota variation among populations of the same animal species (e.g. Chandler et  al. 2011; McKenzie et  al. 2017). Microbial symbionts may therefore contribute to local adaptation (Kawecki and Ebert 2004). Most studies exploring symbiont-mediated local adaptation have focused on vertically transmitted microorganisms (e.g. Moran et al. 2008). However, numerous animals form symbioses wi