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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

S.G. Olvera-Vazquez, C. Remoué, A. Venon, A. Rousselet, O. Grandcolas, M. Azrine, L. Momont, M. Galan, L. Benoit, G. M. David, A. Alhmedi, T. Beliën, G. Alins, P. Franck, A. Haddioui, S.K. Jacobsen, R. Andreev, S. Simon, L. Sigsgaard, E. Guibert, L. Tournant, F. Gazel, K. Mody, Y. Khachtib, A. Roman, T.M. Ursu, I.A. Zakharov, H. Belcram, M. Harry, M. Roth, J.C. Simon, S. Oram, J.M. Ricard, A. Agnello, E. H. Beers, J. Engelman, I. Balti, A. Salhi-Hannachi, H. Zhang, H. Tu, C. Mottet, B. Barrès, A. Degrave, J. Razmjou, T. Giraud, M. Falque, E. Dapena, M. Miñarro, L. Jardillier, P. Deschamps, E. Jousselin, View ORCID ProfileA. Cornille
doi: https://doi.org/10.1101/2020.12.11.421644
S.G. Olvera-Vazquez
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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C. Remoué
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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A. Venon
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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A. Rousselet
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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O. Grandcolas
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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M. Azrine
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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L. Momont
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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M. Galan
2INRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, France
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L. Benoit
2INRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, France
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G. M. David
3Ecologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France
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A. Alhmedi
4Department of Zoology, Fruit Research Center (pcfruit npo), Sint-Truiden, Belgium
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T. Beliën
4Department of Zoology, Fruit Research Center (pcfruit npo), Sint-Truiden, Belgium
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G. Alins
5Institut de Recerca i Tecnologia Agroalimentàries, IRTA-Fruit Production, PCiTAL, Parc de Gardeny, edifici Fruitcentre, 25003 Lleida, Spain
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P. Franck
6INRAE, UR1115, Plantes et Système de cultures Horticoles (PSH), Agroparc CS 40509, Avignon, F-84000, France
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A. Haddioui
7Laboratory of Biotechnology and Valorisation of Plant Genetic Resources, Faculty of Sciences and Techniques, University of Sultan Moulay Slimane, Beni Mellal, Morocco
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S.K. Jacobsen
8Department of Plant and Environmental Sciences, University of Copenhagen, Denmark
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R. Andreev
9Department of Entomology, Agricultural University, Plovdiv, Bulgaria
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S. Simon
10Unité Expérimentale UERI 695, INRAE, 460 Chemin de Gotheron, F-26320 Saint-Marcel-lès-Valence, France
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L. Sigsgaard
8Department of Plant and Environmental Sciences, University of Copenhagen, Denmark
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E. Guibert
11CTIFL, Centre opérationnel de Balandran
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L. Tournant
12Fédération Régionale de Défense contre les Organismes Nuisibles Nord Pas-de-Calais, Loos-en-Gohelle, France
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F. Gazel
13Unité Expérimentale Arboricole - UEA – 0393, INRAE, Bordeaux, France
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K. Mody
14Department of Applied Ecology, Hochschule Geisenheim University, Geisenheim, Germany
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Y. Khachtib
7Laboratory of Biotechnology and Valorisation of Plant Genetic Resources, Faculty of Sciences and Techniques, University of Sultan Moulay Slimane, Beni Mellal, Morocco
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A. Roman
15NIRDBS, Institute of Biological Research Cluj-Napoca, 400015, Cluj-Napoca, Romania
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T.M. Ursu
15NIRDBS, Institute of Biological Research Cluj-Napoca, 400015, Cluj-Napoca, Romania
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I.A. Zakharov
16Vavilov Institute of General Genetics RAS, Moscow, Russia
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H. Belcram
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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M. Harry
17Laboratoire Évolution, Génomes, Comportement, Écologie, UMR9191 CNRS/IRD/Université Paris-Saclay, Gif-sur-Yvette, France
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M. Roth
18GAFL, INRAE, 84140, Montfavet, France
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J.C. Simon
19INRAE, UMR IGEPP, Domaine de la Motte, Le Rheu, France
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S. Oram
20People’s Trust for Endangered Species, London, UK
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J.M. Ricard
11CTIFL, Centre opérationnel de Balandran
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A. Agnello
21Department of Entomology, Cornell AgriTech, Cornell University, Geneva, NY
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E. H. Beers
22Department of Entomology, Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA
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J. Engelman
23Virginia Tech, Alson H. Smith, Jr. Agricultural Research and Extension Center, 595 Laurel Grove Road, Winchester, VA 22602, USA
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I. Balti
24Department of Biology, Faculty of Science of Tunis, University of Tunis El Manar, 2092, Tunis, Tunisia, Salhi-Hannachi A: Department of Biology, Faculty of Science of Tunis, University of Tunis, Tunisia
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A. Salhi-Hannachi
24Department of Biology, Faculty of Science of Tunis, University of Tunis El Manar, 2092, Tunis, Tunisia, Salhi-Hannachi A: Department of Biology, Faculty of Science of Tunis, University of Tunis, Tunisia
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H. Zhang
25Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, 450009, Zhengzhou, China
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H. Tu
25Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, 450009, Zhengzhou, China
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C. Mottet
26Université de Lyon, Anses, INRAE, USC CASPER, 69007 Lyon, France
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B. Barrès
26Université de Lyon, Anses, INRAE, USC CASPER, 69007 Lyon, France
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A. Degrave
27IRHS, INRAE, Agrocampus-Ouest, Université d’Angers, SFR 4207 QUASAV, Beaucouzé, France
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J. Razmjou
28Department of Plant Protection, Faculty of Agriculture and natural Resources, University of Mohaghegh Ardabili, Iran
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T. Giraud
3Ecologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France
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M. Falque
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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E. Dapena
29Servicio Regional de Investigación y Desarrollo Agroalimentario, Ctra. AS-267, PK 19, E-33300, Villaviciosa, Asturias, Spain
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M. Miñarro
29Servicio Regional de Investigación y Desarrollo Agroalimentario, Ctra. AS-267, PK 19, E-33300, Villaviciosa, Asturias, Spain
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L. Jardillier
3Ecologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France
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P. Deschamps
3Ecologie Systematique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France
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E. Jousselin
2INRAE, UMR 1062, Centre de Biologie pour la Gestion des Populations CBGP (INRAE, IRD, CIRAD, Montpellier SupAgro), Montferrier-sur-Lez, 34980, France
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A. Cornille
1Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, 91190 Gif-sur-Yvette, France
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  • ORCID record for A. Cornille
  • For correspondence: amandine.cornille@gmail.com
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Abstract

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.

Competing Interest Statement

The authors of this preprint declare that they have no financial conflict of interest with the content of this article. Amandine Cornille, Tatiana Giraud, Emmanuelle Jousselin, and Jean-Christophe Simon are PCI Evolutionary Ecology Biology recommenders. Tatiana Giraud is a member of the managing board of PCI Evolutionary Biology.

Footnotes

  • The manuscript has been revised according to PCI Evol Biol recommenders. The authors thank the reviewers for their very constructive suggestions.

  • https://zenodo.org/record/4537710#.YCaeomMo95c

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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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
S.G. Olvera-Vazquez, C. Remoué, A. Venon, A. Rousselet, O. Grandcolas, M. Azrine, L. Momont, M. Galan, L. Benoit, G. M. David, A. Alhmedi, T. Beliën, G. Alins, P. Franck, A. Haddioui, S.K. Jacobsen, R. Andreev, S. Simon, L. Sigsgaard, E. Guibert, L. Tournant, F. Gazel, K. Mody, Y. Khachtib, A. Roman, T.M. Ursu, I.A. Zakharov, H. Belcram, M. Harry, M. Roth, J.C. Simon, S. Oram, J.M. Ricard, A. Agnello, E. H. Beers, J. Engelman, I. Balti, A. Salhi-Hannachi, H. Zhang, H. Tu, C. Mottet, B. Barrès, A. Degrave, J. Razmjou, T. Giraud, M. Falque, E. Dapena, M. Miñarro, L. Jardillier, P. Deschamps, E. Jousselin, A. Cornille
bioRxiv 2020.12.11.421644; doi: https://doi.org/10.1101/2020.12.11.421644
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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
S.G. Olvera-Vazquez, C. Remoué, A. Venon, A. Rousselet, O. Grandcolas, M. Azrine, L. Momont, M. Galan, L. Benoit, G. M. David, A. Alhmedi, T. Beliën, G. Alins, P. Franck, A. Haddioui, S.K. Jacobsen, R. Andreev, S. Simon, L. Sigsgaard, E. Guibert, L. Tournant, F. Gazel, K. Mody, Y. Khachtib, A. Roman, T.M. Ursu, I.A. Zakharov, H. Belcram, M. Harry, M. Roth, J.C. Simon, S. Oram, J.M. Ricard, A. Agnello, E. H. Beers, J. Engelman, I. Balti, A. Salhi-Hannachi, H. Zhang, H. Tu, C. Mottet, B. Barrès, A. Degrave, J. Razmjou, T. Giraud, M. Falque, E. Dapena, M. Miñarro, L. Jardillier, P. Deschamps, E. Jousselin, A. Cornille
bioRxiv 2020.12.11.421644; doi: https://doi.org/10.1101/2020.12.11.421644

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