Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification
ABSTRACT The cotton leafworm, Spodoptera littoralis (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 chemosensati...
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2025-03-01
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| Online Access: | https://doi.org/10.1002/ece3.70917 |
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| author | Karine Durand Anne‐Laure Clamens Bruno Le Ru Youssef Dewer Frédérique Hilliou Camille Meslin Nicolas Nègre Gael J. Kergoat Emmanuelle Jacquin‐Joly Kiwoong Nam |
| author_facet | Karine Durand Anne‐Laure Clamens Bruno Le Ru Youssef Dewer Frédérique Hilliou Camille Meslin Nicolas Nègre Gael J. Kergoat Emmanuelle Jacquin‐Joly Kiwoong Nam |
| author_sort | Karine Durand |
| collection | DOAJ |
| description | ABSTRACT The cotton leafworm, Spodoptera littoralis (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 S. littoralis. 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 S. littoralis 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. FST and dXY 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. |
| format | Article |
| id | doaj-art-b8720c526cdf4251830460b876dedcfd |
| institution | OA Journals |
| issn | 2045-7758 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | Wiley |
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| series | Ecology and Evolution |
| spelling | doaj-art-b8720c526cdf4251830460b876dedcfd2025-08-20T01:48:44ZengWileyEcology and Evolution2045-77582025-03-01153n/an/a10.1002/ece3.70917Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in DetoxificationKarine Durand0Anne‐Laure Clamens1Bruno Le Ru2Youssef Dewer3Frédérique Hilliou4Camille Meslin5Nicolas Nègre6Gael J. Kergoat7Emmanuelle Jacquin‐Joly8Kiwoong Nam9DGIMI, INRAE Univ Montpellier Montpellier FranceCBGP, INRAE, CIRAD, IRD, Institut Agro Univ Montpellier Montferrier‐sur‐Lez FranceLaboratoire Evolution Génomes Comportement et Ecologie, UMR CNRS 9191, IRD 247, Université Paris Sud Université Paris‐ Saclay Gif‐sur‐Yvette FrancePhytotoxicity Research Department, Central Agricultural Pesticide Laboratory Agricultural Research Center Giza EgyptINRAE, Institut Sophia Agrobiotech Université Côte D'Azur Nice FranceSorbonne Université, INRAE, CNRS, IRD, UPEC Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris Versailles FranceDGIMI, INRAE Univ Montpellier Montpellier FranceCBGP, INRAE, CIRAD, IRD, Institut Agro Univ Montpellier Montferrier‐sur‐Lez FranceSorbonne Université, INRAE, CNRS, IRD, UPEC Université Paris Cité, Institute of Ecology and Environmental Sciences of Paris Versailles FranceDGIMI, INRAE Univ Montpellier Montpellier FranceABSTRACT The cotton leafworm, Spodoptera littoralis (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 S. littoralis. 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 S. littoralis 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. FST and dXY 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.https://doi.org/10.1002/ece3.70917cotton leafwormcytochrome P450divergent selectionspeciationSpodoptera littoralis |
| spellingShingle | Karine Durand Anne‐Laure Clamens Bruno Le Ru Youssef Dewer Frédérique Hilliou Camille Meslin Nicolas Nègre Gael J. Kergoat Emmanuelle Jacquin‐Joly Kiwoong Nam Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification Ecology and Evolution cotton leafworm cytochrome P450 divergent selection speciation Spodoptera littoralis |
| title | Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification |
| title_full | Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification |
| title_fullStr | Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification |
| title_full_unstemmed | Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification |
| title_short | Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification |
| title_sort | divergent selection promotes intraspecific genomic differentiation in spodoptera littoralis with possible involvement in detoxification |
| topic | cotton leafworm cytochrome P450 divergent selection speciation Spodoptera littoralis |
| url | https://doi.org/10.1002/ece3.70917 |
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