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Dietary change can be a strong evolutionary force and lead to rapid adaptation in organisms. High-fat and high-sugar diets can challenge key metabolic pathways, negatively affecting other life history traits and inducing pathologies such as obesity and diabetes. In this study, we use experimental evolution to investigate the plastic and evolutionary responses to nutritionally unbalanced diets. We reared replicated lines of larvae of the housefly Musca domestica on a fat-enriched (FAT), a sugar-enriched (SUG), and a control (CTRL) diet for thirteen generations. We measured development time in each generation and larval growth and fat accumulation in generations 1, 7, and 13. Subsequently, all lines were reared for one generation on the control diet to detect any plastic and evolutionary changes. In the first generation, time to pupation decreased on a fat-rich diet and increased on a sugar-rich diet. The fat-rich diet increased fat accumulation and, to a lesser extent, the dry weight of the larvae. Multigenerational exposure to unbalanced diets caused compensatory changes in development time, dry weight, and absolute and relative fat content, although pattern and timing depended on diet and trait. When put back on a control diet, many of the changes induced by the unbalanced diets disappeared, indicating that the diet has large plastic effects. Nevertheless, fat-evolved lines still grew significantly larger than the sugar-evolved lines, and sugar-evolved lines had consistently lower fat content. This can be an effect of parental diet or an evolutionary change in nutrient metabolism as a consequence of multigenerational exposure to unbalanced diets., (© The Author(s) 2024. Published by Oxford University Press on behalf of the European Society of Evolutionary Biology.)

The housefly (Musca domestica) is a common insect species with only a few recurrent bacterial taxa in its gut microbiota, because the numerous microbial acquisition routes in its septic habitats can favor transient microbes. Here, we investigated the role of the diet on the microbiota and the developmental success of a housefly strain reared on three substrates. We used a control wheat bran-based substrate, and added clotted cream and sucrose to make a high-fat, and a high-sugar substrate, respectively. The conducted survey revealed that, in contrast to the high-fat diet, the high-sugar diet caused lower developmental success and less diverse microbiota, in which several lactobacilli were replaced with Weissella bacterial phylotypes. Cultures with sucrose as the sole carbon source confirmed that a Weissella confusa strain, isolated from larvae, could utilize sucrose more efficiently than other tested lactic acid bacteria; a result also supported by gene function prediction analysis. Enhancing the rearing substrate with Limosilactobacillus fermentum and Lactiplantibacillus plantarum strains, which were isolated from control larvae, could not only revert the negative effect of the high-sucrose diet on development, but also increase the gut bacterial diversity. In our study, we show that the microbiota shifts in response to the high-sucrose diet did not benefit the host, that showed lower developmental success. In contrast, high-sucrose favored specific components of the microbiota, that continued to be enriched even after multiple generations, outcompeting beneficial bacteria. Also, microbiome manipulation showed the potential of probiotics to rescue host performance and restore the microbiome., (© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)