Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle
| Author(s) | Pélissié, Benjamin | |
| Author(s) | Chen, Yolanda H. | |
| Author(s) | Cohen, Zachary P. | |
| Author(s) | Crossley, Michael S. | |
| Author(s) | Hawthorne, David J. | |
| Author(s) | Izzo, Victor | |
| Author(s) | Schoville, Sean D. | |
| Date Accessioned | 2023-09-22T17:44:07Z | |
| Date Available | 2023-09-22T17:44:07Z | |
| Publication Date | 2022-01-19 | |
| Description | This article was originally published in Molecular Biology and Evolution . The version of record is available at: https://doi.org/10.1093/molbev/msac016. © The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. | |
| Abstract | Insecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices, yet the evolutionary mechanisms that allow pests to rapidly adapt to control tactics remains unclear. Here, we examine how a global super-pest, the Colorado potato beetle (CPB), Leptinotarsa decemlineata, rapidly evolves resistance to insecticides. Using whole-genome resequencing and transcriptomic data focused on its ancestral and pest range in North America, we assess evidence for three, nonmutually exclusive models of rapid evolution: pervasive selection on novel mutations, rapid regulatory evolution, and repeated selection on standing genetic variation. Population genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit similar levels of nucleotide diversity, relative to nonpest populations, and show evidence of recent expansion. Genome scans provide clear signatures of repeated adaptation across CPB populations, with especially strong evidence of selection on insecticide resistance genes in different populations. Analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns. CPB evolves insecticide resistance repeatedly across agricultural regions, leveraging similar genetic pathways but different genes, demonstrating a polygenic trait architecture for insecticide resistance that can evolve from standing genetic variation. Despite expectations, we do not find support for strong selection on novel mutations, or rapid evolution from selection on regulatory genes. These results suggest that integrated pest management practices must mitigate the evolution of polygenic resistance phenotypes among local pest populations, in order to maintain the efficacy and sustainability of novel control techniques. | |
| Sponsor | The authors wish to thank the reviewers and editorial staff for their assistance with our manuscript. The University of Wisconsin Biotechnology Center DNA Sequencing Facility provided essential facilities and services. The authors thank Russell Groves, Justin Clements, Sylvia Rondon, Kristian Brevik, and Andrei Alyokhin for engaging discussions on CPB. Finally, they thank Margarethe Brummerman for help in sampling Leptinotarsa species, and an extensive network of collectors that helped us to collect beetles in the United States, Mexico, and Europe. No ethics approval was required for this research and the authors declare no competing interests. This work was supported by a USDA NIFA AFRI Exploratory Grant (2015-67030-23495), a USDA-National Potato Council award (58-5090-7-073), and two Hatch Awards (WIS02004 and VT-H02010), in addition to support from Wisconsin Potato and Vegetable Growers Association. | |
| Citation | Benjamin Pélissié, Yolanda H Chen, Zachary P Cohen, Michael S Crossley, David J Hawthorne, Victor Izzo, Sean D Schoville, Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle, Molecular Biology and Evolution, Volume 39, Issue 2, February 2022, msac016, https://doi.org/10.1093/molbev/msac016 | |
| ISSN | 1537-1719 | |
| URL | https://udspace.udel.edu/handle/19716/33318 | |
| Language | en_US | |
| Publisher | Molecular Biology and Evolution | |
| Keywords | population genomics | |
| Keywords | insecticide resistance | |
| Keywords | rapid evolution | |
| Keywords | genetic adaptation | |
| Keywords | regulatory evolution | |
| Keywords | insect pest | |
| Keywords | polygenic trait | |
| Keywords | zero hunger | |
| Title | Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle | |
| Type | Article |
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