Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest

Abstract Understanding the spatiotemporal dynamics of pesticide resistance at the landscape scale is essential to anticipate the evolution and spread of new resistance phenotypes. In crop mosaics, host plant specialization in pest populations is likely to dampen the spread of pesticide resistance be...

Full description

Bibliographic Details
Main Authors: Lise Roy, Benoit Barrès, Cécile Capderrey, Frédérique Mahéo, Annie Micoud, Maurice Hullé, Jean‐Christophe Simon
Format: Article
Language:English
Published: Wiley 2022-10-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13417
_version_ 1797989242280869888
author Lise Roy
Benoit Barrès
Cécile Capderrey
Frédérique Mahéo
Annie Micoud
Maurice Hullé
Jean‐Christophe Simon
author_facet Lise Roy
Benoit Barrès
Cécile Capderrey
Frédérique Mahéo
Annie Micoud
Maurice Hullé
Jean‐Christophe Simon
author_sort Lise Roy
collection DOAJ
description Abstract Understanding the spatiotemporal dynamics of pesticide resistance at the landscape scale is essential to anticipate the evolution and spread of new resistance phenotypes. In crop mosaics, host plant specialization in pest populations is likely to dampen the spread of pesticide resistance between different crops even in mobile pests such as aphids. Here, we assessed the contribution of host‐based genetic differentiation to the dynamics of resistance alleles in Myzus persicae, a major aphid pest which displays several insecticide resistance mechanisms. We obtained a representative sample of aphids from a crop mosaic through a suction trap for 7 years and from various crops as a reference collection. We genotyped these aphids at 14 microsatellite markers and four insecticide‐resistant loci, analyzed the genetic structure, and assigned host‐based genetic groups from field‐collected aphids. Four well‐defined genetic clusters were found in aerial samples, three of which with strong association with host‐plants. The fourth group was exclusive to aerial samples and highly divergent from the others, suggesting mixture with a closely related taxon of M. persicae associated with unsampled plants. We found a sharp differentiation between individuals from peach and herbaceous plants. Individuals from herbaceous hosts were separated into two genetic clusters, one more strongly associated with tobacco. The 4‐loci resistance genotypes showed a strong association with the four genetic clusters, indicative of barriers to the spread of resistance. However, we found a small number of clones with resistant alleles on multiple host‐plant species, which may spread insecticide resistance between crops. The 7‐year survey revealed a rapid turn‐over of aphid genotypes as well as the emergence, frequency increase and persistence of clones with resistance to several families of insecticides. This study highlights the importance of considering landscape‐scale population structure to identify the risk of emergence and spread of insecticide resistance for a particular crop.
first_indexed 2024-04-11T08:16:55Z
format Article
id doaj.art-69fa527f47e24067a3da756c3cc15dbf
institution Directory Open Access Journal
issn 1752-4571
language English
last_indexed 2024-04-11T08:16:55Z
publishDate 2022-10-01
publisher Wiley
record_format Article
series Evolutionary Applications
spelling doaj.art-69fa527f47e24067a3da756c3cc15dbf2022-12-22T04:35:07ZengWileyEvolutionary Applications1752-45712022-10-0115101653166910.1111/eva.13417Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pestLise Roy0Benoit Barrès1Cécile Capderrey2Frédérique Mahéo3Annie Micoud4Maurice Hullé5Jean‐Christophe Simon6Université de Lyon, Anses, INRAE, USC CASPER Lyon FranceUniversité de Lyon, Anses, INRAE, USC CASPER Lyon FranceUniversité de Lyon, Anses, INRAE, USC CASPER Lyon FranceINRAE, UMR IGEPP Rennes FranceUniversité de Lyon, Anses, INRAE, USC CASPER Lyon FranceINRAE, UMR IGEPP Rennes FranceINRAE, UMR IGEPP Rennes FranceAbstract Understanding the spatiotemporal dynamics of pesticide resistance at the landscape scale is essential to anticipate the evolution and spread of new resistance phenotypes. In crop mosaics, host plant specialization in pest populations is likely to dampen the spread of pesticide resistance between different crops even in mobile pests such as aphids. Here, we assessed the contribution of host‐based genetic differentiation to the dynamics of resistance alleles in Myzus persicae, a major aphid pest which displays several insecticide resistance mechanisms. We obtained a representative sample of aphids from a crop mosaic through a suction trap for 7 years and from various crops as a reference collection. We genotyped these aphids at 14 microsatellite markers and four insecticide‐resistant loci, analyzed the genetic structure, and assigned host‐based genetic groups from field‐collected aphids. Four well‐defined genetic clusters were found in aerial samples, three of which with strong association with host‐plants. The fourth group was exclusive to aerial samples and highly divergent from the others, suggesting mixture with a closely related taxon of M. persicae associated with unsampled plants. We found a sharp differentiation between individuals from peach and herbaceous plants. Individuals from herbaceous hosts were separated into two genetic clusters, one more strongly associated with tobacco. The 4‐loci resistance genotypes showed a strong association with the four genetic clusters, indicative of barriers to the spread of resistance. However, we found a small number of clones with resistant alleles on multiple host‐plant species, which may spread insecticide resistance between crops. The 7‐year survey revealed a rapid turn‐over of aphid genotypes as well as the emergence, frequency increase and persistence of clones with resistance to several families of insecticides. This study highlights the importance of considering landscape‐scale population structure to identify the risk of emergence and spread of insecticide resistance for a particular crop.https://doi.org/10.1111/eva.13417agricultural landscapegene flowinsecticide resistanceMyzus persicaetemporal dynamics
spellingShingle Lise Roy
Benoit Barrès
Cécile Capderrey
Frédérique Mahéo
Annie Micoud
Maurice Hullé
Jean‐Christophe Simon
Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
Evolutionary Applications
agricultural landscape
gene flow
insecticide resistance
Myzus persicae
temporal dynamics
title Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
title_full Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
title_fullStr Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
title_full_unstemmed Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
title_short Host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
title_sort host plants and insecticides shape the evolution of genetic and clonal diversity in a major aphid crop pest
topic agricultural landscape
gene flow
insecticide resistance
Myzus persicae
temporal dynamics
url https://doi.org/10.1111/eva.13417
work_keys_str_mv AT liseroy hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT benoitbarres hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT cecilecapderrey hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT frederiquemaheo hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT anniemicoud hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT mauricehulle hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest
AT jeanchristophesimon hostplantsandinsecticidesshapetheevolutionofgeneticandclonaldiversityinamajoraphidcroppest