Neotropical bee microbiomes point to a fragmented social core and strong species-level effects

Abstract

Background Individuals that band together create new ecological opportunities for microorganisms. In vertical transmission, theory predicts a conserved microbiota within lineages, especially social bees. Bees exhibit solitary to social behavior among and/or within species, while life cycles can be annual or perennial. Bee nests may be used over generations or only once, and foraging ecology varies widely. To assess which traits are associated with bee microbiomes, we analyzed microbial diversity within solitary and social bees of Apidae, Colletidae, and Halictidae, three bee families in Panama’s tropical forests. Our analysis considered the microbiome of adult gut contents replicated through time, localities, and seasons (wet and dry) and included bee morphology and comparison to abdominal (dissected) microbiota. Diversity and distribution of tropical bee microbes (TBM) within the corbiculate bee clade were emphasized. Results We found the eusocial corbiculate bees tended to possess a more conserved gut microbiome, attributable to vertical transmission, but microbial composition varied among closely related species. Euglossine bees (or orchid bees), corbiculates with mainly solitary behavior, had more variable gut microbiomes. Their shorter-tongued and highly seasonal species displayed greater diversity, attributable to flower-visiting habits. Surprisingly, many stingless bees, the oldest corbiculate clade, lacked bacterial genera thought to predate eusociality, while several facultatively social, and solitary bee species possessed those bacterial taxa. Indeed, nearly all bee species displayed a range of affinities for single or multiple variants of the “socially associated” bacterial taxa, which unexpectedly demonstrated high sequence variation. Conclusions Taken together, these results call into question whether specific bacterial associates facilitate eusocial behavior, or are subsequently adopted, or indicate frequent horizontal transmission between perennial eusocial colonies and other social, facultatively social, and solitary bees.

Influence of social lifestyles on host–microbe symbioses in the bees

“…We also detected the disparity in Wolbachia presence and abundance between social and solitary bees (Table 2), as previously described (De Ramalho et al, 2021;Gerth et al, 2011Gerth et al, , 2015. Further to this, our findings regarding the lack of "corbiculate core" microbes in Euglossini species has been reported since the analysis was undertaken (Kueneman et al, 2023).…”

“…However, the sample size for the Meliponini bees in this analysis was considerably smaller (n = 7), and yet, this core community was detectable. As this study was under review, Kueneman et al, 2023, also failed to detect a stable set of core microbes among orchid bee species, lending further weight to these findings. It should be noted, however, that their findings also suggested that the relationship between the "corbiculate core" and stingless bees also may not be as strong as previously theorised, suggesting a complicated picture that requires further investigation.…”

The Dynamic Changes of Brassica napus Seed Microbiota across the Entire Seed Life in the Field

“…The highest mean of total abundance among all groups was in flower buds (8.22%), followed by 20 daf seeds (6.37%) and young pods (3.99%), and the lowest was in mature seeds (0.31%) ( Table S9 ). Notably, Neisseriaceae is one of the common families in pollinator microbiomes [ 69 , 70 ]. The above findings apply equally to Prevotella 1 and Prevotella 2 [ 69 , 71 ], which were also enriched in flower buds (4.62%), followed by young pods (1.62%), 20 daf seeds (1.59%), and found to be decreased in mature seeds (0.02%).…”

“…Notably, Neisseriaceae is one of the common families in pollinator microbiomes [ 69 , 70 ]. The above findings apply equally to Prevotella 1 and Prevotella 2 [ 69 , 71 ], which were also enriched in flower buds (4.62%), followed by young pods (1.62%), 20 daf seeds (1.59%), and found to be decreased in mature seeds (0.02%).…”

“…They accounted for high relative abundance, especially in the flower stage, and this abundance decreased at the remaining sampling points, with the lowest abundance found in mature seeds. Furthermore, Neisseriaceae and Prevotellaceae are common families among pollinating insects [ 69 , 70 ], and pollinating insects could transmit bacteria into seeds [ 93 ]. All plants were grown naturally in the field, and strict surface sterilization was carried out to rule out human contamination.…”