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To address this significant knowledge gap, we took advantage of the simple, culturable microbiome of\n                    <jats:italic>Drosophila<\/jats:italic>\n                    . First, we documented that natural populations of\n                    <jats:italic>D. simulans<\/jats:italic>\n                    harbor three diverged clades of\n                    <jats:italic>Lactiplantibacillus plantarum<\/jats:italic>\n                    , a key nutritional symbiont. We studied the distinct ecological roles of these three clades by exposing flies with their native microbiome to two temperature regimes in the laboratory. Tracking the three clades within the complete\n                    <jats:italic>Drosophila<\/jats:italic>\n                    microbiome over a period of more than 10 years at two temperatures, we identified strikingly distinct dynamics in response to the selection regime. We confirmed the functional differentiation of the three clades using in vitro growth measurements and in vivo mono-association assays. Our results highlight that environmental selection operates at the subspecies level. 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