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

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...

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Autores principales: Kueneman, Jordan G., Bonadies, Ernesto, Thomas, Devin, Roubik, David W., Wcislo, William T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10347802/
https://www.ncbi.nlm.nih.gov/pubmed/37452376
http://dx.doi.org/10.1186/s40168-023-01593-z
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author Kueneman, Jordan G.
Bonadies, Ernesto
Thomas, Devin
Roubik, David W.
Wcislo, William T.
author_facet Kueneman, Jordan G.
Bonadies, Ernesto
Thomas, Devin
Roubik, David W.
Wcislo, William T.
author_sort Kueneman, Jordan G.
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01593-z.
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spelling pubmed-103478022023-07-15 Neotropical bee microbiomes point to a fragmented social core and strong species-level effects Kueneman, Jordan G. Bonadies, Ernesto Thomas, Devin Roubik, David W. Wcislo, William T. Microbiome Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01593-z. BioMed Central 2023-07-14 /pmc/articles/PMC10347802/ /pubmed/37452376 http://dx.doi.org/10.1186/s40168-023-01593-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Kueneman, Jordan G.
Bonadies, Ernesto
Thomas, Devin
Roubik, David W.
Wcislo, William T.
Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title_full Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title_fullStr Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title_full_unstemmed Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title_short Neotropical bee microbiomes point to a fragmented social core and strong species-level effects
title_sort neotropical bee microbiomes point to a fragmented social core and strong species-level effects
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10347802/
https://www.ncbi.nlm.nih.gov/pubmed/37452376
http://dx.doi.org/10.1186/s40168-023-01593-z
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