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Theoretical frameworks of terrestrial community assembly often focus on single trophic levels (e.g. plants) without considering how complex interdependencies across different trophic levels influence assembly mechanisms. Yet, when multiple trophic levels are considered (e.g. plant–pollinator, plant–microbe interactions) the focus is typically on network analyses at local spatial scales. As spatial variation in biodiversity (β‐diversity) is increasingly being recognized for its relevance in understanding community assembly and conservation, considering how β‐diversity at one trophic level may be influenced by assembly processes that alter abundance and composition of interacting communities at a different trophic level (multitrophic dependency) is critical. Here, we build on single trophic level community assembly frameworks to explore the assembly processes affecting β‐diversity in multitrophic communities comprising flowering plants, their bee pollinators, and the corresponding bee‐gut microbiota to better understand the importance of multitrophic dependency in community assembly. Using distance‐based redundancy analysis and variation partitioning, we investigated community assembly processes across three interconnected trophic levels in two ecological regions in southern California: the Santa Monica Mountains and three islands of the Channel Island Archipelago. We found that the deterministic effects of multitrophic dependency are stronger on directly connected trophic levels than on indirectly connected trophic levels (i.e. flowers explain bee communities and bees explain bee‐gut bacteria communities, but flowers weakly explain variation in bee‐gut bacteria communities). We also found notable regional variation, where multitrophic dependency was weaker on the Channel Islands as ecological drift was more pronounced. Our results suggest that integrating the influence of multitrophic dependency on community assembly is important for elucidating drivers of β‐diversity and that multitrophic dependency can be determined by the regional context in which β‐diversity is measured. Taken together, our results highlight the importance of considering multiscale perspectives – both multitrophic and multiregional – in community assembly to fully elucidate assembly processes. 

ABSTRACT Microbial environmental transmission among individuals plays an important role in shaping the microbiomes of many species. Despite the importance of the microbiome for host fitness, empirical investigations on environmental transmission are scarce, particularly in systems where interactions across multiple trophic levels influence symbiotic dynamics. Here, we explore microbial transmission within insect microbiomes, focusing on solitary bees. Specifically, we investigate the environmental transmission hypothesis, which posits that solitary bees acquire and deposit their associated microbiota from and to their surroundings, especially flowers. Using experimental setups, we examine the transmission dynamics ofApilactobacillus micheneri, a fructophilic and acidophilic bacterium, between the solitary beeOsmia lignaria(Megachilidae) and the plantPhacelia tanacetifolia(Boraginaceae). Our results demonstrate that bees not only acquire bacteria from flowers but also deposit these microbes onto uninoculated flowers for other bees to acquire them, supporting a bidirectional microbial exchange. We therefore find empirical support for the environmental transmission hypothesis, and we discuss the multitrophic dependencies that facilitate microbial transmission between bees and flowers. 

Pathogens and parasites of solitary bees have been studied for decades, but the microbiome as a whole is poorly understood for most taxa. Comparative analyses of microbiome features such as composition, abundance, and specificity, can shed light on bee ecology and the evolution of host–microbe interactions. Here we study microbiomes of ground-nesting cellophane bees (Colletidae: Diphaglossinae). From a microbial point of view, the diphaglossine genus Ptiloglossa is particularly remarkable: their larval provisions are liquid and smell consistently of fermentation. We sampled larval provisions and various life stages from wild nests of Ptiloglossa arizonensis and two species of closely related genera: Caupolicana yarrowi and Crawfordapis luctuosa . We also sampled nectar collected by P. arizonensis . Using 16S rRNA gene sequencing, we find that larval provisions of all three bee species are near-monocultures of lactobacilli. Nectar communities are more diverse, suggesting ecological filtering. Shotgun metagenomic and phylogenetic data indicate that Ptiloglossa culture multiple species and strains of Apilactobacillus , which circulate among bees and flowers. Larval lactobacilli disappear before pupation, and hence are likely not vertically transmitted, but rather reacquired from flowers as adults. Thus, brood cell microbiomes are qualitatively similar between diphaglossine bees and other solitary bees: lactobacilli-dominated, environmentally acquired, and non-species-specific. However, shotgun metagenomes provide evidence of a shift in bacterial abundance. As compared with several other bee species, Ptiloglossa have much higher ratios of bacterial to plant biomass in larval provisions, matching the unusually fermentative smell of their brood cells. Overall, Ptiloglossa illustrate a path by which hosts can evolve quantitatively novel symbioses: not by acquiring or domesticating novel symbionts, but by altering the microenvironment to favor growth of already widespread and generalist microbes.