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Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator

BACKGROUND: The environment is a strong driver of genetic structure in many natural populations, yet often neglected in population genetic studies. This may be a particular problem in vagile species, where subtle structure cannot be explained by limitations to dispersal. Consequently, these species...

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Autores principales: Glück, Marcel, Geue, Julia C., Thomassen, Henri A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8808969/
https://www.ncbi.nlm.nih.gov/pubmed/35105300
http://dx.doi.org/10.1186/s12862-022-01963-5
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author Glück, Marcel
Geue, Julia C.
Thomassen, Henri A.
author_facet Glück, Marcel
Geue, Julia C.
Thomassen, Henri A.
author_sort Glück, Marcel
collection PubMed
description BACKGROUND: The environment is a strong driver of genetic structure in many natural populations, yet often neglected in population genetic studies. This may be a particular problem in vagile species, where subtle structure cannot be explained by limitations to dispersal. Consequently, these species might falsely be considered quasi-panmictic and hence potentially mismanaged. A species this might apply to, is the buff-tailed bumble bee (Bombus terrestris), an economically important and widespread pollinator, which is considered to be quasi-panmictic at mainland continental scales. Here we aimed to (i) quantify genetic structure in 21+ populations of the buff-tailed bumble bee, sampled throughout two Eastern European countries, and (ii) analyse the degree to which structure is explained by environmental differences, habitat permeability and geographic distance. Using 12 microsatellite loci, we characterised populations of this species with Fst analyses, complemented by discriminant analysis of principal components and Bayesian clustering approaches. We then applied generalized dissimilarity modelling to simultaneously assess the informativeness of geographic distance, habitat permeability and environmental differences among populations in explaining divergence. RESULTS: Genetic structure of the buff-tailed bumble bee quantified by means of Fst was subtle and not detected by Bayesian clustering. Discriminant analysis of principal components suggested insignificant but still noticeable structure that slightly exceeded estimates obtained through Fst analyses. As expected, geographic distance and habitat permeability were not informative in explaining the spatial pattern of genetic divergence. Yet, environmental variables related to temperature, vegetation and topography were highly informative, explaining between 33 and 39% of the genetic variation observed. CONCLUSIONS: In contrast to previous studies reporting quasi-panmixia in continental populations of this species, we demonstrated the presence of subtle population structure related to environmental heterogeneity. Environmental data proved to be highly useful in unravelling the drivers of genetic structure in this vagile and opportunistic species. We highlight the potential of including these data to obtain a better understanding of population structure and the processes driving it in species considered to be quasi-panmictic. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01963-5.
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spelling pubmed-88089692022-02-03 Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator Glück, Marcel Geue, Julia C. Thomassen, Henri A. BMC Ecol Evol Research BACKGROUND: The environment is a strong driver of genetic structure in many natural populations, yet often neglected in population genetic studies. This may be a particular problem in vagile species, where subtle structure cannot be explained by limitations to dispersal. Consequently, these species might falsely be considered quasi-panmictic and hence potentially mismanaged. A species this might apply to, is the buff-tailed bumble bee (Bombus terrestris), an economically important and widespread pollinator, which is considered to be quasi-panmictic at mainland continental scales. Here we aimed to (i) quantify genetic structure in 21+ populations of the buff-tailed bumble bee, sampled throughout two Eastern European countries, and (ii) analyse the degree to which structure is explained by environmental differences, habitat permeability and geographic distance. Using 12 microsatellite loci, we characterised populations of this species with Fst analyses, complemented by discriminant analysis of principal components and Bayesian clustering approaches. We then applied generalized dissimilarity modelling to simultaneously assess the informativeness of geographic distance, habitat permeability and environmental differences among populations in explaining divergence. RESULTS: Genetic structure of the buff-tailed bumble bee quantified by means of Fst was subtle and not detected by Bayesian clustering. Discriminant analysis of principal components suggested insignificant but still noticeable structure that slightly exceeded estimates obtained through Fst analyses. As expected, geographic distance and habitat permeability were not informative in explaining the spatial pattern of genetic divergence. Yet, environmental variables related to temperature, vegetation and topography were highly informative, explaining between 33 and 39% of the genetic variation observed. CONCLUSIONS: In contrast to previous studies reporting quasi-panmixia in continental populations of this species, we demonstrated the presence of subtle population structure related to environmental heterogeneity. Environmental data proved to be highly useful in unravelling the drivers of genetic structure in this vagile and opportunistic species. We highlight the potential of including these data to obtain a better understanding of population structure and the processes driving it in species considered to be quasi-panmictic. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01963-5. BioMed Central 2022-02-01 /pmc/articles/PMC8808969/ /pubmed/35105300 http://dx.doi.org/10.1186/s12862-022-01963-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
Glück, Marcel
Geue, Julia C.
Thomassen, Henri A.
Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title_full Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title_fullStr Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title_full_unstemmed Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title_short Environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
title_sort environmental differences explain subtle yet detectable genetic structure in a widespread pollinator
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8808969/
https://www.ncbi.nlm.nih.gov/pubmed/35105300
http://dx.doi.org/10.1186/s12862-022-01963-5
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