Nutritional stress adaptation shapes host microbiome stability and life history dynamics

Abstract

Dietary environments can influence host-microbe evolution by shaping adaptive fitness responses. However, host-microbe dynamics on evolutionary time scales remain under-characterized. We studied Drosophila melanogaster experimentally evolved under three nutrient regimes: constant high (CH), deteriorating (DA), and fluctuating (FA) availability, alongside unselected controls (C). DA and FA increased longevity relative to CH, with DA enhancing late-life survival, though all selected groups showed higher mortality than C, suggesting fitness costs of dietary adaptation. Sex-specific effects emerged, with FA favoring early-life female survival and DA supporting late-life female longevity. Microbial richness and composition shifted with selection and time. While Firmicutes and Proteobacteria dominated generally, selection regimes showed higher Firmicute and lower Proteobacteria abundances compared to C, correlating with dysbiotic microbiomes starting early in adulthood. DA flies maintained a relatively stable microbial diversity over time, potentially supporting longevity. In contrast, CH and FA both exhibited low microbial diversity that destabilized with age. Indicator species analysis revealed treatment- and age-specific genera, with CH and FA showing greater dysbiosis, marked by potentially pathogenic taxa such as Leptotrichia and Mobiluncus. Our findings highlight the importance of early life stages in maintaining microbiome stability and host fitness, suggesting dietary stress drives distinct microbiota patterns and survival strategies.