Independent genetic mapping experiments identify diverse molecular determinants of host adaptation in a generalist herbivore

Interactions between plants and herbivores promote evolutionary change. Studying the evolution of herbivore mechanisms aimed to cope with diUerent host plant species is a critical intersection between evolutionary biology and sustainable pest management. Generalist herbivores are of particular inter...

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Main Authors Villacis-Perez, Ernesto, Graeve, Femke De, Beer, Berdien De, Alshami, Seham Ali, de Jong, Rick, Meyer, Tim De, Leeuwen, Thomas Van
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Published Cold Spring Harbor Laboratory 08.07.2024
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Abstract Interactions between plants and herbivores promote evolutionary change. Studying the evolution of herbivore mechanisms aimed to cope with diUerent host plant species is a critical intersection between evolutionary biology and sustainable pest management. Generalist herbivores are of particular interest, as hybridization between genetically distinct populations can increase the standing genetic variation and therefore the adaptive potential of the species. Tetranychus urticae is a generalist arthropod known for its adaptive potential, evidenced in its immense host range and ability to develop metabolic resistance to xenobiotics. However, the molecular underpinnings associated with the potential of host adaptation and the consequences of host adaptation in this and many other pests remain elusive. Here, we use two independent, empirical approaches to identify and map the genetic basis of host plant performance and adaptation in genetically distinct populations of T. urticae. In the first approach, we subject a genetically diverse mite population to tomato selection and map genomic regions linked to the phenotypic evolution of increased reproductive performance. In the second approach, we map genomic regions responsible for performance on tomato by comparing the genomes of pooled individuals from a F2 backcross between populations with high and low reproductive performance. Both approaches revealed specific and shared genomic regions associated with host plant performance and adaptation and key candidate genes were identified. Our findings highlight the power of spider mite genetic approaches to identify the complex genetic basis of host adaptation in a generalist herbivore.
AbstractList Interactions between plants and herbivores promote evolutionary change. Studying the evolution of herbivore mechanisms aimed to cope with diUerent host plant species is a critical intersection between evolutionary biology and sustainable pest management. Generalist herbivores are of particular interest, as hybridization between genetically distinct populations can increase the standing genetic variation and therefore the adaptive potential of the species. Tetranychus urticae is a generalist arthropod known for its adaptive potential, evidenced in its immense host range and ability to develop metabolic resistance to xenobiotics. However, the molecular underpinnings associated with the potential of host adaptation and the consequences of host adaptation in this and many other pests remain elusive. Here, we use two independent, empirical approaches to identify and map the genetic basis of host plant performance and adaptation in genetically distinct populations of T. urticae. In the first approach, we subject a genetically diverse mite population to tomato selection and map genomic regions linked to the phenotypic evolution of increased reproductive performance. In the second approach, we map genomic regions responsible for performance on tomato by comparing the genomes of pooled individuals from a F2 backcross between populations with high and low reproductive performance. Both approaches revealed specific and shared genomic regions associated with host plant performance and adaptation and key candidate genes were identified. Our findings highlight the power of spider mite genetic approaches to identify the complex genetic basis of host adaptation in a generalist herbivore.
Author Villacis-Perez, Ernesto
Alshami, Seham Ali
Graeve, Femke De
de Jong, Rick
Leeuwen, Thomas Van
Meyer, Tim De
Beer, Berdien De
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  givenname: Ernesto
  orcidid: 0000-0002-0489-8829
  surname: Villacis-Perez
  fullname: Villacis-Perez, Ernesto
  email: thomas.vanleeuwen@ugent.be
  organization: Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University
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  givenname: Femke De
  surname: Graeve
  fullname: Graeve, Femke De
  organization: Department of Data Analysis and Mathematical Modelling, Faculty of Bioscience Engineering, Ghent University
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  givenname: Berdien De
  surname: Beer
  fullname: Beer, Berdien De
  organization: Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University
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  givenname: Seham Ali
  surname: Alshami
  fullname: Alshami, Seham Ali
  organization: Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam (UvA)
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  givenname: Rick
  surname: de Jong
  fullname: de Jong, Rick
  organization: Aeres University of Applied Sciences
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  givenname: Tim De
  surname: Meyer
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  organization: Department of Data Analysis and Mathematical Modelling, Faculty of Bioscience Engineering, Ghent University
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  givenname: Thomas Van
  surname: Leeuwen
  fullname: Leeuwen, Thomas Van
  email: thomas.vanleeuwen@ugent.be
  organization: Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University
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ContentType Paper
Copyright 2024, Posted by Cold Spring Harbor Laboratory
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Keywords experimental evolution – polyphagy – detoxification – chemosensory receptors – quantitative trait loci – transcriptional plasticity
Language English
License This pre-print is available under a Creative Commons License (Attribution-NonCommercial-NoDerivs 4.0 International), CC BY-NC-ND 4.0, as described at http://creativecommons.org/licenses/by-nc-nd/4.0
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Notes Competing Interest Statement: The authors have declared no competing interest.
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Snippet Interactions between plants and herbivores promote evolutionary change. Studying the evolution of herbivore mechanisms aimed to cope with diUerent host plant...
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SubjectTerms Evolutionary Biology
Title Independent genetic mapping experiments identify diverse molecular determinants of host adaptation in a generalist herbivore
URI https://www.biorxiv.org/content/10.1101/2024.07.05.602111
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