Phylosymbiosis with limited functional divergence in bee gut microbiota

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Abstract
Animal microbiomes often show phylosymbiosis, a pattern in which closely related hosts harbour more similar microbial communities than distant hosts. Yet, the processes generating this pattern remain unresolved, particularly whether phylosymbiosis requires sociality and vertical microbial transmission or can emerge through host filtering from environmental microbial pools. Bees (Anthophila) provide a powerful model to test this question because their major evolutionary radiation spans diverse life histories and contrasting microbiome transmission modes. Here, we analysed gut bacterial communities from 60 bee genera worldwide (1,989 samples), spanning all major bee families, and combined comparative phylogenetic models with host traits, bacterial phylogenies and predicted functional profiles to disentangle ecological and evolutionary drivers of phylosymbiosis. We found strong phylosymbiosis across and within bee families, with host phylogeny explaining substantial variation in gut microbiome composition despite weak effects of measured host traits. Geo-environmental context also explained considerable variation, indicating interactions between evolutionary and environmental filters. Despite extensive taxonomic and phylogenetic turnover, microbial functional divergence was weaker, suggesting convergence despite compositional differentiation. Together, these results show that microbiome composition can follow host phylogeny even under predominantly environmental acquisition and that phylosymbiosis can emerge through repeated assembly of functionally conserved communities rather than strict microbial inheritance.

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