Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa

With frequent host shifts involving the colonization of new hosts across large geographical ranges, crop pests are good models for examining the mechanisms of rapid colonization. The microbial partners of pest insects may also be involved in or affected by colonization processes, which has been litt...

Full description

Bibliographic Details
Main Authors: Olvera-Vazquez, S.G., Remoué, C., Venon, A., Rousselet, A., Grandcolas, O., Azrine, M., Momont, L., Galan, M., Benoit, L., David, G. M., Alhmedi, A., Beliën, T., Alins, G., Franck, P., Haddioui, A., Jacobsen, S.K., Andreev, R., Simon, S., Sigsgaard, L., Guibert, E., Tournant, L., Gazel, F., Mody, K., Khachtib, Y., Roman, A., Ursu, T.M., Zakharov, I.A., Belcram, H., Harry, M., Roth, M., Simon, J.C., Oram, S., Ricard, J.M., Agnello, A., Beers, E. H., Engelman, J., Balti, I., Salhi-Hannachi, A., Zhang, H., Tu, H., Mottet, C., Barrès, B., Degrave, A., Razmjou, J., Giraud, T., Falque, M., Dapena, E., Miñarro, M., Jardillier, L., Deschamps, P., Jousselin, E., Cornille, A.
Format: Article
Language:English
Published: Peer Community In 2021-11-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.26/
_version_ 1797651201223819264
author Olvera-Vazquez, S.G.
Remoué, C.
Venon, A.
Rousselet, A.
Grandcolas, O.
Azrine, M.
Momont, L.
Galan, M.
Benoit, L.
David, G. M.
Alhmedi, A.
Beliën, T.
Alins, G.
Franck, P.
Haddioui, A.
Jacobsen, S.K.
Andreev, R.
Simon, S.
Sigsgaard, L.
Guibert, E.
Tournant, L.
Gazel, F.
Mody, K.
Khachtib, Y.
Roman, A.
Ursu, T.M.
Zakharov, I.A.
Belcram, H.
Harry, M.
Roth, M.
Simon, J.C.
Oram, S.
Ricard, J.M.
Agnello, A.
Beers, E. H.
Engelman, J.
Balti, I.
Salhi-Hannachi, A.
Zhang, H.
Tu, H.
Mottet, C.
Barrès, B.
Degrave, A.
Razmjou, J.
Giraud, T.
Falque, M.
Dapena, E.
Miñarro, M.
Jardillier, L.
Deschamps, P.
Jousselin, E.
Cornille, A.
author_facet Olvera-Vazquez, S.G.
Remoué, C.
Venon, A.
Rousselet, A.
Grandcolas, O.
Azrine, M.
Momont, L.
Galan, M.
Benoit, L.
David, G. M.
Alhmedi, A.
Beliën, T.
Alins, G.
Franck, P.
Haddioui, A.
Jacobsen, S.K.
Andreev, R.
Simon, S.
Sigsgaard, L.
Guibert, E.
Tournant, L.
Gazel, F.
Mody, K.
Khachtib, Y.
Roman, A.
Ursu, T.M.
Zakharov, I.A.
Belcram, H.
Harry, M.
Roth, M.
Simon, J.C.
Oram, S.
Ricard, J.M.
Agnello, A.
Beers, E. H.
Engelman, J.
Balti, I.
Salhi-Hannachi, A.
Zhang, H.
Tu, H.
Mottet, C.
Barrès, B.
Degrave, A.
Razmjou, J.
Giraud, T.
Falque, M.
Dapena, E.
Miñarro, M.
Jardillier, L.
Deschamps, P.
Jousselin, E.
Cornille, A.
author_sort Olvera-Vazquez, S.G.
collection DOAJ
description With frequent host shifts involving the colonization of new hosts across large geographical ranges, crop pests are good models for examining the mechanisms of rapid colonization. The microbial partners of pest insects may also be involved in or affected by colonization processes, which has been little studied so far. We investigated the demographic history of the rosy apple aphid, Dysaphis plantaginea, a major pest of the cultivated apple (Malus domestica) in Europe, North Africa and North America, as well as the diversity of its microbiota. We genotyped a comprehensive sample of 714 colonies from Europe, Morocco and the US using mitochondrial (CytB and CO1), bacterial (16s rRNA and TrnpB), and 30 microsatellite markers. We detected five populations spread across the US, Morocco, Western and Eastern Europe and Spain. Populations showed weak genetic differentiation and high genetic diversity, except the ones from Morocco and North America that are likely the result of recent colonization events. Coalescent-based inferences revealed high levels of gene flow among populations during the colonization but did not allow determining the sequence of colonization of Europe, North America and Morroco by D. plantaginea, likely because of the weak genetic differentiation and the occurrence of gene flow among populations. We found that D. plantaginea rarely hosts other endosymbiotic bacteria than its obligate nutritional symbiont Buchnera aphidicola. This suggests that secondary endosymbionts did not play an important role in the rapid spread of the rosy apple aphid. These findings have fundamental importance for understanding pest colonization processes and implications for sustainable pest control programs.
first_indexed 2024-03-11T16:11:28Z
format Article
id doaj.art-addfd8a9fae54cd580ca2227bb67c950
institution Directory Open Access Journal
issn 2804-3871
language English
last_indexed 2024-03-11T16:11:28Z
publishDate 2021-11-01
publisher Peer Community In
record_format Article
series Peer Community Journal
spelling doaj.art-addfd8a9fae54cd580ca2227bb67c9502023-10-24T14:38:25ZengPeer Community InPeer Community Journal2804-38712021-11-01110.24072/pcjournal.2610.24072/pcjournal.26Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North AfricaOlvera-Vazquez, S.G.0https://orcid.org/0000-0002-2826-6957Remoué, C.1Venon, A.2Rousselet, A.3Grandcolas, O.4Azrine, M.5Momont, L.6Galan, M.7Benoit, L.8David, G. M.9Alhmedi, A.10Beliën, T.11Alins, G.12Franck, P.13Haddioui, A.14Jacobsen, S.K.15Andreev, R.16Simon, S.17Sigsgaard, L.18Guibert, E.19Tournant, L.20Gazel, F.21Mody, K.22Khachtib, Y.23Roman, A.24Ursu, T.M.25Zakharov, I.A.26Belcram, H.27Harry, M.28Roth, M.29Simon, J.C.30Oram, S.31Ricard, J.M.32Agnello, A.33Beers, E. H.34Engelman, J.35Balti, I.36Salhi-Hannachi, A.37Zhang, H.38Tu, H.39Mottet, C.40Barrès, B.41Degrave, A.42Razmjou, J.43Giraud, T.44Falque, M.45Dapena, E.46Miñarro, M.47Jardillier, L.48Deschamps, P.49Jousselin, E.50Cornille, A.51https://orcid.org/0000-0002-5348-7081Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceINRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, FranceINRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, FranceEcologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, FranceDepartment of Zoology, Fruit Research Center (Pcfruit Npo), Sint-Truiden, BelgiumDepartment of Zoology, Fruit Research Center (Pcfruit Npo), Sint-Truiden, BelgiumInstitut de Recerca i Tecnologia Agroalimentàries, IRTA-Fruit Production, PCiTAL, Parc de Gardeny, edifici Fruitcentre, 25003 Lleida, SpainINRAE, UR1115, Plantes et Système de cultures Horticoles (PSH), Agroparc CS 40509, Avignon, F-84000, FranceLaboratory of Biotechnology and Valorisation of Plant Genetic Resources, Faculty of Sciences and Techniques, University of Sultan Moulay Slimane, Beni Mellal, MoroccoDepartment of Plant and Environmental Sciences, University of Copenhagen, DenmarkDepartment of Entomology, Agricultural University, Plovdiv, BulgariaUnité Expérimentale UERI 695, INRAE, 460 Chemin de Gotheron, F-26320 Saint-Marcel-lès-Valence, FranceDepartment of Plant and Environmental Sciences, University of Copenhagen, DenmarkCTIFL, Centre opérationnel de Balandran, Bellegarde, FranceFédération Régionale de Défense contre les Organismes Nuisibles Nord Pas-de-Calais, Loos-en-Gohelle, FranceUnité Expérimentale Arboricole - UEA – 0393, INRAE, Bordeaux, FranceDepartment of Applied Ecology, Hochschule Geisenheim University, Geisenheim, GermanyLaboratory of Biotechnology and Valorisation of Plant Genetic Resources, Faculty of Sciences and Techniques, University of Sultan Moulay Slimane, Beni Mellal, MoroccoNIRDBS, Institute of Biological Research Cluj-Napoca, 400015, Cluj-Napoca, RomaniaNIRDBS, Institute of Biological Research Cluj-Napoca, 400015, Cluj-Napoca, RomaniaVavilov Institute of General Genetics RAS, Moscow, RussiaUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceLaboratoire Évolution, Génomes, Comportement, Écologie, UMR9191 CNRS/IRD/Université Paris-Saclay, Gif-sur-Yvette, FranceGAFL, INRAE, 84140, Montfavet, FranceINRAE, UMR IGEPP, Domaine de la Motte, Le Rheu, FrancePeople's Trust for Endangered Species, London, UKCTIFL, Centre opérationnel de Balandran, Bellegarde, FranceDepartment of Entomology, Cornell AgriTech, Cornell University, Geneva, NY, USADepartment of Entomology, Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, USAVirginia Tech, Alson H. Smith, Jr. Agricultural Research and Extension Center, 595 Laurel Grove Road, Winchester, VA 22602, USADepartment of Biology, Faculty of Science of Tunis, University of Tunis El Manar, 2092, Tunis, TunisiaDepartment of Biology, Faculty of Science of Tunis, University of Tunis El Manar, 2092, Tunis, TunisiaZhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, 450009, Zhengzhou, ChinaZhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, 450009, Zhengzhou, ChinaUniversité de Lyon, Anses, INRAE, USC CASPER, 69007 Lyon, FranceUniversité de Lyon, Anses, INRAE, USC CASPER, 69007 Lyon, FranceIRHS, INRAE, Agrocampus-Ouest, Université d’Angers, SFR 4207 QUASAV, Beaucouzé, FranceDepartment of Plant Protection, Faculty of Agriculture and natural Resources, University of Mohaghegh Ardabili, IranEcologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceServicio Regional de Investigación y Desarrollo Agroalimentario, Ctra. AS-267, PK 19, E-33300, Villaviciosa, Asturias, SpainServicio Regional de Investigación y Desarrollo Agroalimentario, Ctra. AS-267, PK 19, E-33300, Villaviciosa, Asturias, SpainEcologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, FranceEcologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, FranceINRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, FranceUniversité Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, FranceWith frequent host shifts involving the colonization of new hosts across large geographical ranges, crop pests are good models for examining the mechanisms of rapid colonization. The microbial partners of pest insects may also be involved in or affected by colonization processes, which has been little studied so far. We investigated the demographic history of the rosy apple aphid, Dysaphis plantaginea, a major pest of the cultivated apple (Malus domestica) in Europe, North Africa and North America, as well as the diversity of its microbiota. We genotyped a comprehensive sample of 714 colonies from Europe, Morocco and the US using mitochondrial (CytB and CO1), bacterial (16s rRNA and TrnpB), and 30 microsatellite markers. We detected five populations spread across the US, Morocco, Western and Eastern Europe and Spain. Populations showed weak genetic differentiation and high genetic diversity, except the ones from Morocco and North America that are likely the result of recent colonization events. Coalescent-based inferences revealed high levels of gene flow among populations during the colonization but did not allow determining the sequence of colonization of Europe, North America and Morroco by D. plantaginea, likely because of the weak genetic differentiation and the occurrence of gene flow among populations. We found that D. plantaginea rarely hosts other endosymbiotic bacteria than its obligate nutritional symbiont Buchnera aphidicola. This suggests that secondary endosymbionts did not play an important role in the rapid spread of the rosy apple aphid. These findings have fundamental importance for understanding pest colonization processes and implications for sustainable pest control programs.https://peercommunityjournal.org/articles/10.24072/pcjournal.26/
spellingShingle Olvera-Vazquez, S.G.
Remoué, C.
Venon, A.
Rousselet, A.
Grandcolas, O.
Azrine, M.
Momont, L.
Galan, M.
Benoit, L.
David, G. M.
Alhmedi, A.
Beliën, T.
Alins, G.
Franck, P.
Haddioui, A.
Jacobsen, S.K.
Andreev, R.
Simon, S.
Sigsgaard, L.
Guibert, E.
Tournant, L.
Gazel, F.
Mody, K.
Khachtib, Y.
Roman, A.
Ursu, T.M.
Zakharov, I.A.
Belcram, H.
Harry, M.
Roth, M.
Simon, J.C.
Oram, S.
Ricard, J.M.
Agnello, A.
Beers, E. H.
Engelman, J.
Balti, I.
Salhi-Hannachi, A.
Zhang, H.
Tu, H.
Mottet, C.
Barrès, B.
Degrave, A.
Razmjou, J.
Giraud, T.
Falque, M.
Dapena, E.
Miñarro, M.
Jardillier, L.
Deschamps, P.
Jousselin, E.
Cornille, A.
Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
Peer Community Journal
title Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
title_full Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
title_fullStr Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
title_full_unstemmed Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
title_short Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa
title_sort large scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in europe north america and north africa
url https://peercommunityjournal.org/articles/10.24072/pcjournal.26/
work_keys_str_mv AT olveravazquezsg largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT remouec largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT venona largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT rousseleta largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT grandcolaso largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT azrinem largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT momontl largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT galanm largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT benoitl largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT davidgm largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT alhmedia largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT belient largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT alinsg largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT franckp largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT haddiouia largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT jacobsensk largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT andreevr largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT simons largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT sigsgaardl largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT guiberte largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT tournantl largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT gazelf largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT modyk largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT khachtiby largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT romana largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT ursutm largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT zakharovia largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT belcramh largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT harrym largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT rothm largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT simonjc largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT orams largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT ricardjm largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT agnelloa largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT beerseh largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT engelmanj largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT baltii largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT salhihannachia largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT zhangh largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT tuh largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT mottetc largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT barresb largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT degravea largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT razmjouj largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT giraudt largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT falquem largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT dapenae largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT minarrom largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT jardillierl largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT deschampsp largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT jousseline largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica
AT cornillea largescalegeographysurveyprovidesinsightsintothecolonizationhistoryofamajoraphidpestonitscultivatedapplehostineuropenorthamericaandnorthafrica