Microbiota have emerged as fundamental regulators of host physiology, shaping both ecological interactions and evolutionary trajectories. Yet, the determinants of microbiota diversity and structure in wild populations—particularly the respective roles of host genetics and environmental context—are still poorly understood. In this study, we investigated these influences in the freshwater snail Bulinus truncatus, a key intermediate host for human and animal Schistosoma parasites, using a multifactorial approach. We developed 31 new microsatellite markers to resolve population genetic structure across nine sites in Senegal. Metabarcoding methods were then employed to profile the bacterial microbiota of individual snails and to characterize environmental bacterial assemblages from each location via environmental DNA. Shell measurements and molecular diagnostics for trematode infection status were included to assess additional potential contributors. Employing multiple regression on distance matrices (MRM), we quantified how snail population genetics, site-specific environmental bacterial communities, spatial patterns, and infection status shape microbiota composition. Our analyses reveal that snail geographic distribution and population genetic structure drive the composition of Bulinus truncatus microbiota, with environmental bacterial communities exerting a weaker but still significant effect. In contrast, neither shell size nor trematode infection status impacted microbiota structure significantly. Notably, a considerable fraction of variation remains unexplained, indicating the likely involvement of other ecological or intrinsic factors. These results advance understanding of microbiota determinants in natural populations and underscore the intricate interplay between host genetics, environment, and microbial communities.

Microbiota are increasingly recognized as key players in regulating host biological functions, influencing both the ecology and evolution of organisms. However, the factors shaping microbiota diversity and structure in natural environments remain underexplored, especially the relative importance of host genetics versus environmental factors. In this study, we address this gap using the freshwater snail Bulinus truncatus, an intermediate host for some human and animal Schistosoma parasites, as a model species. We developed 31 new microsatellite markers to assess the population structure of B. truncatus across 9 sites in Senegal. We then applied metabarcoding to characterize the diversity and structure of individual snail bacterial microbiota and environmental communities associated with each sampling site using environmental DNA. We also used molecular diagnostics to determine trematode infection status of B. truncatus individuals. By integrating these data through multiple regression on distance matrices (MRM) analyses, we quantified the influence of B. truncatus population genetics, spatial distribution, environmental bacterial communities, and infection status on the snail’s microbiota structure. Our results show that the genetic structure of B. truncatus populations, and to a lower extent geographic distribution, are the main factors explaining the snail’s microbiota compositions. Neither the environmental bacterial communities nor trematode infection status significantly contributed to microbiota structure. A portion of the variance in microbiota composition remains unexplained, suggesting that additional ecological or intrinsic factors might be involved. These findings provide new insights into the drivers of microbiota structure in natural populations and highlight the complexity of host-microbiota-environment interactions.