Phylosymbiosis and functional redundancy in the Drosophila (Diptera: Drosophilidae) gut microbiome and its implications for host fitness

The gut microbiome plays a fundamental role in host ecophysiology. Numerous studies have examined microbiome composition and functionality to understand the ecological and evolutionary factors shaping host-microbe interactions. However, the consequences of these patterns for animal ecology remain poorly understood. Here, we examined how variations in the gut microbiome influence fitness differences among Drosophila species sharing a common dietary niche. Using 16S rRNA gene sequencing, we analyzed the gut microbial taxonomy and predicted functional profiles of 4 Drosophila species collected in central Chile. Our results revealed a strong signal of phylosymbiosis in the microbial taxonomy, while functionality was highly redundant across the studied fly species. Functional biomarkers analysis indicated that the gut microbiome supports the nutritional requirements of D. simulans (Sturtevant), D. hydei (Sturtevant), and D. repleta (Wollaston); whereas, this was less evident in D. melanogaster (Meigen). To assess the potential contribution of the microbiome to host performance, we compared egg-to-adult viability between 2 species with the greatest physiological divergence: D. simulans and D. hydei. Notably, D. simulans exhibited significantly higher egg viability and shorter development time than D. hydei. Strikingly, the D. simulans microbiome contained more taxonomic and functional biomarkers previously demonstrated to enhance fly fitness, whereas the D. hydei microbiome harbored taxa and functions potentially detrimental to host performance. These findings suggest that the gut microbiome contributes to host fitness and may shape the evolutionary ecology of Drosophila species, with broader implications for community dynamics, including interspecific competition and species displacement.