Section: Evolutionary Biology
Topic: Evolution, Population biology

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

10.24072/pcjournal.26 - Peer Community Journal, Volume 1 (2021), article no. e34.

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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.

Published online:
DOI: 10.24072/pcjournal.26
Type: Research article
Olvera-Vazquez, S.G. 1; Remoué, C. 1; Venon, A. 1; Rousselet, A. 1; Grandcolas, O. 1; Azrine, M. 1; Momont, L. 1; Galan, M. 2; Benoit, L. 2; David, G. M. 3; Alhmedi, A. 4; Beliën, T. 4; Alins, G. 5; Franck, P. 6; Haddioui, A. 7; Jacobsen, S.K. 8; Andreev, R. 9; Simon, S. 10; Sigsgaard, L. 8; Guibert, E. 11; Tournant, L. 12; Gazel, F. 13; Mody, K. 14; Khachtib, Y. 7; Roman, A. 15; Ursu, T.M. 15; Zakharov, I.A. 16; Belcram, H. 1; Harry, M. 17; Roth, M. 18; Simon, J.C. 19; Oram, S. 20; Ricard, J.M. 11; Agnello, A. 21; Beers, E. H. 22; Engelman, J. 23; Balti, I. 24; Salhi-Hannachi, A. 24; Zhang, H. 25; Tu, H. 25; Mottet, C. 26; Barrès, B. 26; Degrave, A. 27; Razmjou, J. 28; Giraud, T. 3; Falque, M. 1; Dapena, E. 29; Miñarro, M. 29; Jardillier, L. 3; Deschamps, P. 3; Jousselin, E. 2; Cornille, A. 1

1 Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
2 INRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, France
3 Ecologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France
4 Department of Zoology, Fruit Research Center (Pcfruit Npo), Sint-Truiden, Belgium
5 Institut de Recerca i Tecnologia Agroalimentàries, IRTA-Fruit Production, PCiTAL, Parc de Gardeny, edifici Fruitcentre, 25003 Lleida, Spain
6 INRAE, UR1115, Plantes et Système de cultures Horticoles (PSH), Agroparc CS 40509, Avignon, F-84000, France
7 Laboratory of Biotechnology and Valorisation of Plant Genetic Resources, Faculty of Sciences and Techniques, University of Sultan Moulay Slimane, Beni Mellal, Morocco
8 Department of Plant and Environmental Sciences, University of Copenhagen, Denmark
9 Department of Entomology, Agricultural University, Plovdiv, Bulgaria
10 Unité Expérimentale UERI 695, INRAE, 460 Chemin de Gotheron, F-26320 Saint-Marcel-lès-Valence, France
11 CTIFL, Centre opérationnel de Balandran, Bellegarde, France
12 Fédération Régionale de Défense contre les Organismes Nuisibles Nord Pas-de-Calais, Loos-en-Gohelle, France
13 Unité Expérimentale Arboricole - UEA – 0393, INRAE, Bordeaux, France
14 Department of Applied Ecology, Hochschule Geisenheim University, Geisenheim, Germany
15 NIRDBS, Institute of Biological Research Cluj-Napoca, 400015, Cluj-Napoca, Romania
16 Vavilov Institute of General Genetics RAS, Moscow, Russia
17 Laboratoire Évolution, Génomes, Comportement, Écologie, UMR9191 CNRS/IRD/Université Paris-Saclay, Gif-sur-Yvette, France
18 GAFL, INRAE, 84140, Montfavet, France
19 INRAE, UMR IGEPP, Domaine de la Motte, Le Rheu, France
20 People's Trust for Endangered Species, London, UK
21 Department of Entomology, Cornell AgriTech, Cornell University, Geneva, NY, USA
22 Department of Entomology, Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, USA
23 Virginia Tech, Alson H. Smith, Jr. Agricultural Research and Extension Center, 595 Laurel Grove Road, Winchester, VA 22602, USA
24 Department of Biology, Faculty of Science of Tunis, University of Tunis El Manar, 2092, Tunis, Tunisia
25 Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, 450009, Zhengzhou, China
26 Université de Lyon, Anses, INRAE, USC CASPER, 69007 Lyon, France
27 IRHS, INRAE, Agrocampus-Ouest, Université d’Angers, SFR 4207 QUASAV, Beaucouzé, France
28 Department of Plant Protection, Faculty of Agriculture and natural Resources, University of Mohaghegh Ardabili, Iran
29 Servicio Regional de Investigación y Desarrollo Agroalimentario, Ctra. AS-267, PK 19, E-33300, Villaviciosa, Asturias, Spain
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Olvera-Vazquez, S.G. and Remou\'e, C. and Venon, A. and Rousselet, A. and Grandcolas, O. and Azrine, M. and Momont, L. and Galan, M. and Benoit, L. and David, G. M. and Alhmedi, A. and Beli\"en, T. and Alins, G. and Franck, P. and Haddioui, A. and Jacobsen, S.K. and Andreev, R. and Simon, S. and Sigsgaard, L. and Guibert, E. and Tournant, L. and Gazel, F. and Mody, K. and Khachtib, Y. and Roman, A. and Ursu, T.M. and Zakharov, I.A. and Belcram, H. and Harry, M. and Roth, M. and Simon, J.C. and Oram, S. and Ricard, J.M. and Agnello, A. and Beers, E. H. and Engelman, J. and Balti, I. and Salhi-Hannachi, A. and Zhang, H. and Tu, H. and Mottet, C. and Barr\`es, B. and Degrave, A. and Razmjou, J. and Giraud, T. and Falque, M. and Dapena, E. and Mi\~narro, M. and Jardillier, L. and Deschamps, P. and Jousselin, E. and Cornille, A.},
     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}},
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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, Volume 1 (2021), article  no. e34. doi : 10.24072/pcjournal.26.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100134

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