Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae

Abstract The rapid evolution of pesticide resistance imposes great pressure on food production. However, how resistance alleles arise and spread across field populations remains largely understood. Here, we study the evolutionary trajectories of resistance alleles in Tetranychus urticae, a rapidly e...

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Main Authors: Lei Chen, Li-Xue Guo, Hua-Meng Zhang, Xiao-Nan Sun, Yu-Ting Liu, Jie Ji, Wen-Xin Xue, Nicky Wybouw, Thomas Van Leeuwen, Xiao-Feng Xue, Xiao-Yue Hong, Jing-Tao Sun
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-08658-9
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author Lei Chen
Li-Xue Guo
Hua-Meng Zhang
Xiao-Nan Sun
Yu-Ting Liu
Jie Ji
Wen-Xin Xue
Nicky Wybouw
Thomas Van Leeuwen
Xiao-Feng Xue
Xiao-Yue Hong
Jing-Tao Sun
author_facet Lei Chen
Li-Xue Guo
Hua-Meng Zhang
Xiao-Nan Sun
Yu-Ting Liu
Jie Ji
Wen-Xin Xue
Nicky Wybouw
Thomas Van Leeuwen
Xiao-Feng Xue
Xiao-Yue Hong
Jing-Tao Sun
author_sort Lei Chen
collection DOAJ
description Abstract The rapid evolution of pesticide resistance imposes great pressure on food production. However, how resistance alleles arise and spread across field populations remains largely understood. Here, we study the evolutionary trajectories of resistance alleles in Tetranychus urticae, a rapidly evolving pest. We sequence the genomes of 258 T. urticae females collected from China. Combined with global reference genomic data, we examine the evolutionary origin(s) of 18 mutations across 10 target-site genes and analyze the global population genetic structure using genome-wide SNPs. Our findings reveal a striking prevalence of multiple independent origins of resistance mutations, with only two of 18 mutations showing an apparent single origin. Population structure and haplotype analyses point to an important role of gene flow in the spread of resistance alleles. Selection analyses reveal pesticide-driven sweeps affecting genetic diversity. These findings advance our understanding of the rapid adaptation of arthropod herbivores to extreme selective pressure.
format Article
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institution Kabale University
issn 2399-3642
language English
publishDate 2025-08-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-dcb9310078a740878e3dd8bdfffa3c342025-08-20T03:46:19ZengNature PortfolioCommunications Biology2399-36422025-08-018111710.1038/s42003-025-08658-9Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticaeLei Chen0Li-Xue Guo1Hua-Meng Zhang2Xiao-Nan Sun3Yu-Ting Liu4Jie Ji5Wen-Xin Xue6Nicky Wybouw7Thomas Van Leeuwen8Xiao-Feng Xue9Xiao-Yue Hong10Jing-Tao Sun11Department of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityInstitute of Plant Protection, Fujian Academy of Agricultural SciencesTobacco Research Institute, Chinese Academy of Agricultural SciencesDepartment of Biology, Faculty of Sciences, Ghent UniversityLaboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent UniversityDepartment of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityDepartment of Entomology, Nanjing Agricultural UniversityAbstract The rapid evolution of pesticide resistance imposes great pressure on food production. However, how resistance alleles arise and spread across field populations remains largely understood. Here, we study the evolutionary trajectories of resistance alleles in Tetranychus urticae, a rapidly evolving pest. We sequence the genomes of 258 T. urticae females collected from China. Combined with global reference genomic data, we examine the evolutionary origin(s) of 18 mutations across 10 target-site genes and analyze the global population genetic structure using genome-wide SNPs. Our findings reveal a striking prevalence of multiple independent origins of resistance mutations, with only two of 18 mutations showing an apparent single origin. Population structure and haplotype analyses point to an important role of gene flow in the spread of resistance alleles. Selection analyses reveal pesticide-driven sweeps affecting genetic diversity. These findings advance our understanding of the rapid adaptation of arthropod herbivores to extreme selective pressure.https://doi.org/10.1038/s42003-025-08658-9
spellingShingle Lei Chen
Li-Xue Guo
Hua-Meng Zhang
Xiao-Nan Sun
Yu-Ting Liu
Jie Ji
Wen-Xin Xue
Nicky Wybouw
Thomas Van Leeuwen
Xiao-Feng Xue
Xiao-Yue Hong
Jing-Tao Sun
Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
Communications Biology
title Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
title_full Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
title_fullStr Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
title_full_unstemmed Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
title_short Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae
title_sort population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest tetranychus urticae
url https://doi.org/10.1038/s42003-025-08658-9
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