Divergent Selection Promotes Intraspecific Genomic Differentiation in <i>Spodoptera littoralis</i> With Possible Involvement in Detoxification

The cotton leafworm, <i>Spodoptera littoralis</i> (Lepidoptera: Noctuidae), is a major agricultural pest affecting crops like cotton, maize, tomatoes, and wheat across southern Europe, Africa, the Middle East, and western Asia. Whole genome analyses have revealed adaptive evolution in chemosensation and detoxification genes in <i>S. littoralis</i>. However, the extent of intraspecific diversity influenced by recent adaptive evolutionary forces remains unclear. In this study, we conducted a population genomics analysis using 31 <i>S. littoralis</i> individuals from sub-Saharan Africa, northern Africa, and southern Europe to assess the existence of intraspecific population divergence and identify the underlying evolutionary forces. We show whole genome differentiation between populations based on geographic origin from the analyzed samples. Phylogenetic analyses indicate that sub-Saharan and southern European populations share a common ancestor, distinct from several northern African populations. F<sub>ST</sub> and d<sub>XY</sub> statistics along the chromosomes reveal loci with restricted gene flow among populations. These loci are associated with population-specific selective sweeps, indicating the role of divergent natural selection in limiting gene flow. Notably, these loci are enriched with detoxification genes, including cytochrome P450, multidrug resistance, and xanthine dehydrogenase genes, all of which are potentially associated with detoxification. These results demonstrate that divergent selection limits gene flow among geographically distinct populations with the possibility of the involvement of detoxification as a key trait. We argue that this genetic heterogeneity can be considered in pest monitoring and management, as strategies tailored to specific populations may not be relevant for others.

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Journal
Ecology and Evolution
Published
2025-03-01
DOI
https://doi.org/10.1002/ece3.70917
Primary Topic
Insect Resistance and Genetics
Type
article
Field-Weighted Citation Impact
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article

Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification

Anne‐Laure Clamens, Youssef Dewer, Frédérique Hilliou, Emmanuelle Jacquin‐Joly et al.
Ecology and Evolution
Insect Resistance and Genetics
article

Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification

Anne‐Laure Clamens, Youssef Dewer, Frédérique Hilliou, Emmanuelle Jacquin‐Joly, Karine Durand, Camille Meslin, Nicolas Nègre, Kiwoong Nam, Gaël J. Kergoat, Bruno Le Rü
article en

Abstract

The cotton leafworm, <i>Spodoptera littoralis</i> (Lepidoptera: Noctuidae), is a major agricultural pest affecting crops like cotton, maize, tomatoes, and wheat across southern Europe, Africa, the Middle East, and western Asia. Whole genome analyses have revealed adaptive evolution in chemosensation and detoxification genes in <i>S. littoralis</i>. However, the extent of intraspecific diversity influenced by recent adaptive evolutionary forces remains unclear. In this study, we conducted a population genomics analysis using 31 <i>S. littoralis</i> individuals from sub-Saharan Africa, northern Africa, and southern Europe to assess the existence of intraspecific population divergence and identify the underlying evolutionary forces. We show whole genome differentiation between populations based on geographic origin from the analyzed samples. Phylogenetic analyses indicate that sub-Saharan and southern European populations share a common ancestor, distinct from several northern African populations. F<sub>ST</sub> and d<sub>XY</sub> statistics along the chromosomes reveal loci with restricted gene flow among populations. These loci are associated with population-specific selective sweeps, indicating the role of divergent natural selection in limiting gene flow. Notably, these loci are enriched with detoxification genes, including cytochrome P450, multidrug resistance, and xanthine dehydrogenase genes, all of which are potentially associated with detoxification. These results demonstrate that divergent selection limits gene flow among geographically distinct populations with the possibility of the involvement of detoxification as a key trait. We argue that this genetic heterogeneity can be considered in pest monitoring and management, as strategies tailored to specific populations may not be relevant for others.

Ecology and EvolutionVol. 15(3)
Université Paris-Sud (FR), Centre National de la Recherche Scientifique (FR), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR), International Centre of Insect Physiology and Ecology (KE), Université Paris-Est Créteil (FR), Université de Montpellier (FR), Université Paris Cité (FR), Institut Agro Montpellier (FR), Agropolis International (FR), Université Paris-Saclay (FR), Sorbonne Université (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Évolution, Génomes, Comportement, Écologie (FR), Diversité, génomes et interactions micro-organismes-insectes (FR), Central Laboratory For Agricultural Expert Systems (EG), Institut d'écologie et des sciences de l'environnement de Paris (FR), Centre de Biologie pour la Gestion des Populations (FR), Institut Sophia Agrobiotech (FR), Agricultural Research Center (EG), Institut de Recherche pour le Développement (FR), L'Institut Agro (FR)
Agence Nationale de la Recherche, South African Sugarcane Research Institute
Life in Land
Openalex Percentile: Top 95%
Insect Resistance and Genetics
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