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The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator

The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop species. Agricultural ecosystems typically have very different abiotic and ecological conditions from th...

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Autores principales: Pope, Nathaniel S., Singh, Avehi, Childers, Anna K., Kapheim, Karen M., Evans, Jay D., López-Uribe, Margarita M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104555/
https://www.ncbi.nlm.nih.gov/pubmed/37011184
http://dx.doi.org/10.1073/pnas.2208116120
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author Pope, Nathaniel S.
Singh, Avehi
Childers, Anna K.
Kapheim, Karen M.
Evans, Jay D.
López-Uribe, Margarita M.
author_facet Pope, Nathaniel S.
Singh, Avehi
Childers, Anna K.
Kapheim, Karen M.
Evans, Jay D.
López-Uribe, Margarita M.
author_sort Pope, Nathaniel S.
collection PubMed
description The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop species. Agricultural ecosystems typically have very different abiotic and ecological conditions from those they replaced and create potential niches for those species that are able to exploit the abundant resources offered by crop plants. While there are well-studied examples of crop pests that have adapted into novel agricultural niches, the impact of agricultural intensification on the evolution of crop mutualists such as pollinators is poorly understood. We combined genealogical inference from genomic data with archaeological records to demonstrate that the Holocene demographic history of a wild specialist pollinator of Cucurbita (pumpkins, squashes, and gourds) has been profoundly impacted by the history of agricultural expansion in North America. Populations of the squash bee Eucera pruinosa experienced rapid growth in areas where agriculture intensified within the past 1,000 y, suggesting that the cultivation of Cucurbita in North America has increased the amount of floral resources available to these bees. In addition, we found that roughly 20% of this bee species’ genome shows signatures of recent selective sweeps. These signatures are overwhelmingly concentrated in populations from eastern North America where squash bees were historically able to colonize novel environments due to human cultivation of Cucurbita pepo and now exclusively inhabit agricultural niches. These results suggest that the widespread cultivation of crops can prompt adaptation in wild pollinators through the distinct ecological conditions imposed by agricultural environments.
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spelling pubmed-101045552023-04-15 The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator Pope, Nathaniel S. Singh, Avehi Childers, Anna K. Kapheim, Karen M. Evans, Jay D. López-Uribe, Margarita M. Proc Natl Acad Sci U S A Biological Sciences The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop species. Agricultural ecosystems typically have very different abiotic and ecological conditions from those they replaced and create potential niches for those species that are able to exploit the abundant resources offered by crop plants. While there are well-studied examples of crop pests that have adapted into novel agricultural niches, the impact of agricultural intensification on the evolution of crop mutualists such as pollinators is poorly understood. We combined genealogical inference from genomic data with archaeological records to demonstrate that the Holocene demographic history of a wild specialist pollinator of Cucurbita (pumpkins, squashes, and gourds) has been profoundly impacted by the history of agricultural expansion in North America. Populations of the squash bee Eucera pruinosa experienced rapid growth in areas where agriculture intensified within the past 1,000 y, suggesting that the cultivation of Cucurbita in North America has increased the amount of floral resources available to these bees. In addition, we found that roughly 20% of this bee species’ genome shows signatures of recent selective sweeps. These signatures are overwhelmingly concentrated in populations from eastern North America where squash bees were historically able to colonize novel environments due to human cultivation of Cucurbita pepo and now exclusively inhabit agricultural niches. These results suggest that the widespread cultivation of crops can prompt adaptation in wild pollinators through the distinct ecological conditions imposed by agricultural environments. National Academy of Sciences 2023-04-03 2023-04-11 /pmc/articles/PMC10104555/ /pubmed/37011184 http://dx.doi.org/10.1073/pnas.2208116120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Pope, Nathaniel S.
Singh, Avehi
Childers, Anna K.
Kapheim, Karen M.
Evans, Jay D.
López-Uribe, Margarita M.
The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title_full The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title_fullStr The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title_full_unstemmed The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title_short The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
title_sort expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104555/
https://www.ncbi.nlm.nih.gov/pubmed/37011184
http://dx.doi.org/10.1073/pnas.2208116120
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