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Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees

SIMPLE SUMMARY: Our study investigated the dynamics of pathogen communities within Chinese bumblebee populations, a key issue for understanding emerging infectious diseases and their impacts on insect biodiversity loss. By employing computational modeling on extensive pathogen data from bumblebees,...

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Autores principales: Chen, Huanhuan, Zhang, Guangshuo, Ding, Guiling, Huang, Jiaxing, Zhang, Hong, Vidal, Mayra C., Corlett, Richard T., Liu, Cong, An, Jiandong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672019/
https://www.ncbi.nlm.nih.gov/pubmed/37999086
http://dx.doi.org/10.3390/insects14110887
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author Chen, Huanhuan
Zhang, Guangshuo
Ding, Guiling
Huang, Jiaxing
Zhang, Hong
Vidal, Mayra C.
Corlett, Richard T.
Liu, Cong
An, Jiandong
author_facet Chen, Huanhuan
Zhang, Guangshuo
Ding, Guiling
Huang, Jiaxing
Zhang, Hong
Vidal, Mayra C.
Corlett, Richard T.
Liu, Cong
An, Jiandong
author_sort Chen, Huanhuan
collection PubMed
description SIMPLE SUMMARY: Our study investigated the dynamics of pathogen communities within Chinese bumblebee populations, a key issue for understanding emerging infectious diseases and their impacts on insect biodiversity loss. By employing computational modeling on extensive pathogen data from bumblebees, we uncover that the host species variation significantly influences pathogen assembly and occurrences, compared to environmental factors like climate and location. Moreover, our results reveal significant pathogen–pathogen interactions, with similar pathogens exhibiting facilitatory relationships and distinct pathogen types showing strong negative associations, possibly due to immune response interactions and competitive dynamics within hosts. Our findings highlight the role of host–pathogen coevolution and other ecological interactions in shaping pathogen communities. The implications of this work are substantial for bumblebee conservation, improving our understanding of pathogen dynamics that could inform strategies to stop declines in bumblebee populations. ABSTRACT: Bumblebees have been considered one of the most important pollinators on the planet. However, recent reports of bumblebee decline have raised concern about a significant threat to ecosystem stability. Infectious diseases caused by multiple pathogen infections have been increasingly recognized as an important mechanism behind this decline worldwide. Understanding the determining factors that influence the assembly and composition of pathogen communities among bumblebees can provide important implications for predicting infectious disease dynamics and making effective conservation policies. Here, we study the relative importance of biotic interactions versus interspecific host resistance in shaping the pathogen community composition of bumblebees in China. We first conducted a comprehensive survey of 13 pathogens from 22 bumblebee species across China. We then applied joint species distribution modeling to assess the determinants of pathogen community composition and examine the presence and strength of pathogen–pathogen associations. We found that host species explained most of the variations in pathogen occurrences and composition, suggesting that host specificity was the most important variable in predicting pathogen occurrences and community composition in bumblebees. Moreover, we detected both positive and negative associations among pathogens, indicating the role of competition and facilitation among pathogens in determining pathogen community assembly. Our research demonstrates the power of a pluralistic framework integrating field survey of bumblebee pathogens with community ecology frameworks to understand the underlying mechanisms of pathogen community assembly.
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spelling pubmed-106720192023-11-17 Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees Chen, Huanhuan Zhang, Guangshuo Ding, Guiling Huang, Jiaxing Zhang, Hong Vidal, Mayra C. Corlett, Richard T. Liu, Cong An, Jiandong Insects Article SIMPLE SUMMARY: Our study investigated the dynamics of pathogen communities within Chinese bumblebee populations, a key issue for understanding emerging infectious diseases and their impacts on insect biodiversity loss. By employing computational modeling on extensive pathogen data from bumblebees, we uncover that the host species variation significantly influences pathogen assembly and occurrences, compared to environmental factors like climate and location. Moreover, our results reveal significant pathogen–pathogen interactions, with similar pathogens exhibiting facilitatory relationships and distinct pathogen types showing strong negative associations, possibly due to immune response interactions and competitive dynamics within hosts. Our findings highlight the role of host–pathogen coevolution and other ecological interactions in shaping pathogen communities. The implications of this work are substantial for bumblebee conservation, improving our understanding of pathogen dynamics that could inform strategies to stop declines in bumblebee populations. ABSTRACT: Bumblebees have been considered one of the most important pollinators on the planet. However, recent reports of bumblebee decline have raised concern about a significant threat to ecosystem stability. Infectious diseases caused by multiple pathogen infections have been increasingly recognized as an important mechanism behind this decline worldwide. Understanding the determining factors that influence the assembly and composition of pathogen communities among bumblebees can provide important implications for predicting infectious disease dynamics and making effective conservation policies. Here, we study the relative importance of biotic interactions versus interspecific host resistance in shaping the pathogen community composition of bumblebees in China. We first conducted a comprehensive survey of 13 pathogens from 22 bumblebee species across China. We then applied joint species distribution modeling to assess the determinants of pathogen community composition and examine the presence and strength of pathogen–pathogen associations. We found that host species explained most of the variations in pathogen occurrences and composition, suggesting that host specificity was the most important variable in predicting pathogen occurrences and community composition in bumblebees. Moreover, we detected both positive and negative associations among pathogens, indicating the role of competition and facilitation among pathogens in determining pathogen community assembly. Our research demonstrates the power of a pluralistic framework integrating field survey of bumblebee pathogens with community ecology frameworks to understand the underlying mechanisms of pathogen community assembly. MDPI 2023-11-17 /pmc/articles/PMC10672019/ /pubmed/37999086 http://dx.doi.org/10.3390/insects14110887 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Chen, Huanhuan
Zhang, Guangshuo
Ding, Guiling
Huang, Jiaxing
Zhang, Hong
Vidal, Mayra C.
Corlett, Richard T.
Liu, Cong
An, Jiandong
Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title_full Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title_fullStr Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title_full_unstemmed Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title_short Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees
title_sort interspecific host variation and biotic interactions drive pathogen community assembly in chinese bumblebees
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672019/
https://www.ncbi.nlm.nih.gov/pubmed/37999086
http://dx.doi.org/10.3390/insects14110887
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