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
;
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
10.24072/pcjournal.26 - Peer Community Journal, Volume 1 (2021), article no. e34.
Get full text PDF Peer reviewed and recommended by PCI
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.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_26,
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}},
journal = {Peer Community Journal},
eid = {e34},
publisher = {Peer Community In},
volume = {1},
year = {2021},
doi = {10.24072/pcjournal.26},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.26/}
}
TY - JOUR AU - Olvera-Vazquez, S.G. AU - Remoué, C. AU - Venon, A. AU - Rousselet, A. AU - Grandcolas, O. AU - Azrine, M. AU - Momont, L. AU - Galan, M. AU - Benoit, L. AU - David, G. M. AU - Alhmedi, A. AU - Beliën, T. AU - Alins, G. AU - Franck, P. AU - Haddioui, A. AU - Jacobsen, S.K. AU - Andreev, R. AU - Simon, S. AU - Sigsgaard, L. AU - Guibert, E. AU - Tournant, L. AU - Gazel, F. AU - Mody, K. AU - Khachtib, Y. AU - Roman, A. AU - Ursu, T.M. AU - Zakharov, I.A. AU - Belcram, H. AU - Harry, M. AU - Roth, M. AU - Simon, J.C. AU - Oram, S. AU - Ricard, J.M. AU - Agnello, A. AU - Beers, E. H. AU - Engelman, J. AU - Balti, I. AU - Salhi-Hannachi, A. AU - Zhang, H. AU - Tu, H. AU - Mottet, C. AU - Barrès, B. AU - Degrave, A. AU - Razmjou, J. AU - Giraud, T. AU - Falque, M. AU - Dapena, E. AU - Miñarro, M. AU - Jardillier, L. AU - Deschamps, P. AU - Jousselin, E. AU - Cornille, A. TI - 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 JO - Peer Community Journal PY - 2021 VL - 1 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.26/ DO - 10.24072/pcjournal.26 ID - 10_24072_pcjournal_26 ER -
%0 Journal Article %A Olvera-Vazquez, S.G. %A Remoué, C. %A Venon, A. %A Rousselet, A. %A Grandcolas, O. %A Azrine, M. %A Momont, L. %A Galan, M. %A Benoit, L. %A David, G. M. %A Alhmedi, A. %A Beliën, T. %A Alins, G. %A Franck, P. %A Haddioui, A. %A Jacobsen, S.K. %A Andreev, R. %A Simon, S. %A Sigsgaard, L. %A Guibert, E. %A Tournant, L. %A Gazel, F. %A Mody, K. %A Khachtib, Y. %A Roman, A. %A Ursu, T.M. %A Zakharov, I.A. %A Belcram, H. %A Harry, M. %A Roth, M. %A Simon, J.C. %A Oram, S. %A Ricard, J.M. %A Agnello, A. %A Beers, E. H. %A Engelman, J. %A Balti, I. %A Salhi-Hannachi, A. %A Zhang, H. %A Tu, H. %A Mottet, C. %A Barrès, B. %A Degrave, A. %A Razmjou, J. %A Giraud, T. %A Falque, M. %A Dapena, E. %A Miñarro, M. %A Jardillier, L. %A Deschamps, P. %A Jousselin, E. %A Cornille, A. %T 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 %J Peer Community Journal %D 2021 %V 1 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.26/ %R 10.24072/pcjournal.26 %F 10_24072_pcjournal_26
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. https://peercommunityjournal.org/articles/10.24072/pcjournal.26/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100134
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] The oriental fruitfly Bactrocera dorsalis s.s. in East Asia: disentangling the different forces promoting the invasion and shaping the genetic make-up of populations, Genetica, Volume 142 (2014) no. 3, pp. 201-213 | DOI
[2] Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | DOI
[3] What Do We Really Know About Adaptation at Range Edges?, Annual Review of Ecology, Evolution, and Systematics, Volume 51 (2020) no. 1, pp. 341-361 | DOI
[4] Fruit tree Aphids and their natural enemies in Isparta region,Turkey, Journal of Pest Science, Volume 78 (2005) no. 4, pp. 227-229 | DOI
[5] Evolution of Coalescence Times, Genetic Diversity and Structure during Colonization, Theoretical Population Biology, Volume 51 (1997) no. 2, pp. 148-164 | DOI
[6] IPM case studies: deciduous fruit tree aphids., Aphids as crop pests, CABI, Wallingford, 2007, pp. 632-642 | DOI
[7] Indo-European origins: A computer-simulation test of five hypotheses, American Journal of Physical Anthropology, Volume 96 (1995) no. 2, pp. 109-132 | DOI
[8] Phylogenetic relationships of Dysaphis pyri (Boyer de Fonscolombe) and Dysaphis reaumuri (Mordvilko) (Hemiptera, Sternorrhyncha: Aphididae): COI and EF-1α evidence, Organisms Diversity & Evolution, Volume 12 (2012) no. 2, pp. 197-204 | DOI
[9] ABC as a flexible framework to estimate demography over space and time: some cons, many pros, Molecular Ecology, Volume 19 (2010) no. 13, pp. 2609-2625 | DOI
[10] Aphids on the world’s crops: An identification and information guide, John Wiley & Sons Ltd, 2000
[11] Founder effects and species introductions: A host versus parasite perspective, Evolutionary Applications, Volume 13 (2020) no. 3, pp. 559-574 | DOI
[12] Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt., Aphididae) on plantain and as migrant to apple, Journal of Pest Science, Volume 77 (2004) no. 3 | DOI
[13] Three roads diverged? Routes to phylogeographic inference, Trends in Ecology & Evolution, Volume 25 (2010) no. 11, pp. 626-632 | DOI
[14] Le puceron cendré du pommier (Dysaphis plantaginea Pass.). Morphologie et biologie. Méthodes de lutte, Annales Des Épiphyties, Volume 3 (1959)
[15] Worldwide Populations of the Aphid Aphis craccivora Are Infected with Diverse Facultative Bacterial Symbionts, Microbial Ecology, Volume 67 (2014) no. 1, pp. 195-204 | DOI
[16] Machine Learning, 45 (2001) no. 1, pp. 5-32 | DOI
[17] Endosymbiosis of animals with plant microorganisms, Interscience Publishers, New York, 1965
[18] Dysaphis plantaginea. [Distribution map]. Nosworthy Way, Wallingford, Oxfordshire, OX10 8DE, UK.: CAB International Wallingford UK. Retrieved from https://www.cabi.org/isc/abstract/20056600429, 2020
[19] Update on comparative genome mapping between Malus and Pyrus, BMC Research Notes, Volume 2 (2009) no. 1 | DOI
[20] A young age of subspecific divergence in the desert locust inferred by ABC random forest, Molecular Ecology, Volume 29 (2020) no. 23, pp. 4542-4558 | DOI
[21] Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study, Molecular Ecology Notes, Volume 7 (2007) no. 5, pp. 747-756 | DOI
[22] Molecular phylogeny of Macrosiphini (Hemiptera: Aphididae): An evolutionary hypothesis for the Pterocomma-group habitat adaptation, Molecular Phylogenetics and Evolution, Volume 121 (2018), pp. 12-22 | DOI
[23] A Multifaceted Overview of Apple Tree Domestication, Trends in Plant Science, Volume 24 (2019) no. 8, pp. 770-782 | DOI
[24] Anthropogenic and natural drivers of gene flow in a temperate wild fruit tree: a basis for conservation and breeding programs in apples, Evolutionary Applications, Volume 8 (2015) no. 4, pp. 373-384 | DOI
[25] The domestication and evolutionary ecology of apples, Trends in Genetics, Volume 30 (2014) no. 2, pp. 57-65 | DOI
[26] Description and Power Analysis of Two Tests for Detecting Recent Population Bottlenecks From Allele Frequency Data, Genetics, Volume 144 (1996) no. 4, pp. 2001-2014 | DOI
[27] abc: an R package for approximate Bayesian computation (ABC), Methods in Ecology and Evolution, Volume 3 (2012) no. 3, pp. 475-479 | DOI
[28] Approximate Bayesian Computation (ABC) in practice, Trends in Ecology & Evolution, Volume 25 (2010) no. 7, pp. 410-418 | DOI
[29] The effect of the Neolithic expansion on European molecular diversity, Proceedings of the Royal Society B: Biological Sciences, Volume 272 (2005) no. 1564, pp. 679-688 | DOI
[30] Theade4Package: Implementing the Duality Diagram for Ecologists, Journal of Statistical Software, Volume 22 (2007) no. 4 | DOI
[31] (2009). Tess version 2.3—Reference Manual August 2009. Available at memberstimc.imag.fr/Olivier, 2009
[32] Standard and generalized McDonald-Kreitman test: a website to detect selection by comparing different classes of DNA sites, Nucleic Acids Research, Volume 36 (2008) | DOI
[33] FROGS: Find, Rapidly, OTUs with Galaxy Solution, Bioinformatics, Volume 34 (2018) no. 8, pp. 1287-1294 | DOI
[34] Reconstructing routes of invasion using genetic data: why, how and so what?, Molecular Ecology, Volume 19 (2010) no. 19, pp. 4113-4130 | DOI
[35] Model choice using Approximate Bayesian Computation and Random Forests: analyses based on model grouping to make inferences about the genetic history of Pygmy human populations, Journal de la Société Française de Statistique, Volume 159 (2018)
[36] Detecting the number of clusters of individuals using the software structure: a simulation study, Molecular Ecology, Volume 14 (2005) no. 8, pp. 2611-2620 | DOI
[37] fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios, Bioinformatics, Volume 27 (2011) no. 9, pp. 1332-1334 | DOI
[38] Genetic Consequences of Range Expansions, Annual Review of Ecology, Evolution, and Systematics, Volume 40 (2009) no. 1, pp. 481-501 | DOI
[39] Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Molecular Ecology Resources, Volume 10 (2010) no. 3, pp. 564-567 | DOI
[40] Genetic origin and dispersal of the invasive soybean aphid inferred from population genetic analysis and approximate Bayesian computation, Integrative Zoology, Volume 13 (2018) no. 5, pp. 536-552 | DOI
[41] Biological and genetic features of introduced aphid populations in agroecosystems, Current Opinion in Insect Science, Volume 26 (2018), pp. 63-68 | DOI
[42] Gene Frequency Clines Produced by Kin-Structured Founder Effects, Human Biology, Volume 69 (1997)
[43] Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew, Plasmopara viticola, Current Biology, Volume 31 (2021) no. 10 | DOI
[44] Adventive aphids (Hemiptera: Aphididae) of America north of Mexico, Proceedings of the Entomological Society of Washington, Volume 108 (2006)
[45] Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles, Nature Communications, Volume 8 (2017) no. 1 | DOI
[46] Microbial symbionts of herbivorous species across the insect tree, Advances in Insect Physiology, Elsevier, 2020, pp. 111-159 | DOI
[47] Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest, Molecular Biology and Evolution | DOI
[48] pophelper: an R package and web app to analyse and visualize population structure, Molecular Ecology Resources, Volume 17 (2016) no. 1, pp. 27-32 | DOI
[49] Demographic History of European Populations of Arabidopsis thaliana, PLoS Genetics, Volume 4 (2008) no. 5 | DOI
[50] Statistical Tests of Neutrality of Mutations Against Population Growth, Hitchhiking and Background Selection, Genetics, Volume 147 (1997) no. 2, pp. 915-925 | DOI
[51] Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences, Biological Invasions, Volume 18 (2016) no. 4, pp. 935-952 | DOI
[52] Detection of reduction in population size using data from microsatellite loci, Molecular Ecology, Volume 10 (2001) no. 2, pp. 305-318 | DOI
[53] Bacterial Communities Associated with Host-Adapted Populations of Pea Aphids Revealed by Deep Sequencing of 16S Ribosomal DNA, PLOS ONE, Volume 10 (2015) no. 3 | DOI
[54] Dysaphis plantaginea (Passerini, 1860) in GBIF Secretariat. GBIF Backbone Taxonomy. Checklist dataset https://doi.org/10.15468/39omei accessed via GBIF.org on 2021-10-29, 2020
[55] Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest, Insect Biochemistry and Molecular Biology, Volume 120 (2020) | DOI
[56] The population biology of fungal invasions, Molecular Ecology, Volume 24 (2015) no. 9, pp. 1969-1986 | DOI
[57] Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes, Molecular Ecology, Volume 23 (2014) no. 4, pp. 753-773 | DOI
[58] An evaluation of genetic distances for use with microsatellite loci., Genetics, Volume 139 (1995) no. 1, pp. 463-471 | DOI
[59] Weak Spatial and Temporal Population Genetic Structure in the Rosy Apple Aphid, Dysaphis plantaginea, in French Apple Orchards, PLoS ONE, Volume 6 (2011) no. 6 | DOI
[60] spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels, Molecular Ecology Notes, Volume 2 (2002) no. 4, pp. 618-620 | DOI
[61] Genetic clues to the origin of the apple, Trends in Genetics, Volume 18 (2002) no. 8, pp. 426-430 | DOI
[62] Diversity of Bacteria Associated with Natural AphidPopulations, Applied and Environmental Microbiology, Volume 69 (2003) no. 12, pp. 7216-7223 | DOI
[63] Insect life history and the evolution of bacterial mutualism, Ecology Letters, Volume 18 (2015) no. 6, pp. 516-525 | DOI
[64] Phylogeography’s past, present, and future: 10 years after Avise, 2000, Molecular Phylogenetics and Evolution, Volume 54 (2010) no. 1, pp. 291-301 | DOI
[65] Biological invasions and natural colonisations: are they that different?, NeoBiota, Volume 29 (2016), pp. 1-14 | DOI
[66] Host Plant Catalog of Aphids, Springer Netherlands, Dordrecht, 2009 | DOI
[67] MRBAYES: Bayesian inference of phylogenetic trees, Bioinformatics, Volume 17 (2001) no. 8, pp. 754-755 | DOI
[68] CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure, Bioinformatics, Volume 23 (2007) no. 14, pp. 1801-1806 | DOI
[69] A tutorial for Discriminant Analysis of Principal Components (DAPC) using adegenet 2.0.0. 43. Retrieved from http://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf. London: Imperial College London, MRC Centre for Outbreak Analysis and Modelling, 2015
[70] Discriminant analysis of principal components: a new method for the analysis of genetically structured populations, BMC Genetics, Volume 11 (2010) no. 1 | DOI
[71] Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus, Molecular Ecology Resources, Volume 16 (2016) no. 3, pp. 628-640 | DOI
[72] Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola : bacterial genome helps define species and evolutionary relationships in aphids, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1654, pp. 187-196 | DOI
[73] About the aphid fauna (Homoptera Aphididae) of West Tien-Shan (Kazakhstan part), Tethys Entomological Research, Volume 4 (2002)
[74] The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure, Heredity, Volume 106 (2011) no. 4, pp. 625-632 | DOI
[75] Population genetics of the soybean aphid in North America and East Asia: test for introduction between native and introduced populations, Biological Invasions, Volume 19 (2016) no. 2, pp. 597-614 | DOI
[76] Molecular genetics and genomics generate new insights into invertebrate pest invasions, Evolutionary Applications, Volume 6 (2013) no. 5, pp. 842-856 | DOI
[77] Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform, Applied and Environmental Microbiology, Volume 79 (2013) no. 17, pp. 5112-5120 | DOI
[78] MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Molecular Biology and Evolution, Volume 33 (2016) no. 7, pp. 1870-1874 | DOI
[79] Ecological genetics of invasive alien species, BioControl, Volume 56 (2011) no. 4, pp. 409-428 | DOI
[80] A Link Between Communities of Protective Endosymbionts and Parasitoids of the Pea Aphid Revealed in Unmanipulated Agricultural Systems, Frontiers in Ecology and Evolution, Volume 9 (2021) | DOI
[81] Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host, Evolutionary Ecology, Volume 30 (2016) no. 5, pp. 925-941 | DOI
[82] Endosymbionts facilitate rapid evolution in a polyphagous herbivore, Journal of Evolutionary Biology, Volume 33 (2020) no. 10, pp. 1507-1511 | DOI
[83] Spatial genetic structure of a tropical understory shrub, PSYCHOTRIA OFFICINALIS (RuBIACEAE), American Journal of Botany, Volume 82 (1995) no. 11, pp. 1420-1425 | DOI
[84] Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybirdHarmonia axyridis, Molecular Ecology, Volume 23 (2014) no. 24, pp. 5979-5997 | DOI
[85] The relative importance of short- and long-range movement of flying aphids, Biological Reviews, Volume 68 (1993) no. 2, pp. 291-311 | DOI
[86] FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, Volume 27 (2011) no. 21, pp. 2957-2963 | DOI
[87] Swarm: robust and fast clustering method for amplicon-based studies, PeerJ, Volume 2 (2014) | DOI
[88] Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI
[89] Adaptive protein evolution at the Adh locus in Drosophila, Nature, Volume 351 (1991) no. 6328, pp. 652-654 | DOI
[90] genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms, Molecular Ecology Notes, Volume 4 no. 4, pp. 792-794 | DOI
[91] Synthetic Maps of Human Gene Frequencies in Europeans, Science, Volume 201 (1978) no. 4358, pp. 786-792 | DOI
[92] Taxonomic Classification of Bacterial 16S rRNA Genes Using Short Sequencing Reads: Evaluation of Effective Study Designs, PLoS ONE, Volume 8 (2013) no. 1 | DOI
[93] Contrasting population structure and demographic history of cereal aphids in different environmental and agricultural landscapes, Ecology and Evolution, Volume 10 (2020) no. 18, pp. 9647-9662 | DOI
[94] Molecular Evolutionary Genetics, Columbia University Press, 1987 | DOI
[95] Facultative Symbionts in Aphids and the Horizontal Transfer of Ecologically Important Traits, Annual Review of Entomology, Volume 55 (2009) no. 1, pp. 247-266 | DOI
[96] Host range expansion of an introduced insect pest through multiple colonizations of specialized clones, Molecular Ecology, Volume 17 (2008) no. 21, pp. 4608-4618 | DOI
[97] Regular or covert sex defines two lineages and worldwide superclones within the leaf-curl plum aphid (Brachycaudus helichrysi, Kaltenbach), Molecular Ecology, Volume 22 (2013) no. 15, pp. 3916-3932 | DOI
[98] Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data, Journal of Heredity, Volume 90 (1999) no. 4, pp. 502-503 | DOI
[99] Large-scale phylogeographic study of the cosmopolitan aphid pestBrachycaudus helichrysireveals host plant associated lineages that evolved in allopatry, Biological Journal of the Linnean Society, Volume 120 (2016) | DOI
[100] Intraspecific gene genealogies: trees grafting into networks, Trends in Ecology & Evolution, Volume 16 (2001) no. 1, pp. 37-45 | DOI
[101] Inference of Population Structure Using Multilocus Genotype Data, Genetics, Volume 155 (2000) no. 2 | DOI
[102] Geography predicts neutral genetic diversity of human populations, Current Biology, Volume 15 (2005) no. 5 | DOI
[103] Reliable ABC model choice via random forests, Bioinformatics, Volume 32 (2016) no. 6, pp. 859-866 | DOI
[104] The programstructuredoes not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem, Molecular Ecology Resources, Volume 16 (2016) no. 3, pp. 608-627 | DOI
[105] ABC random forests for Bayesian parameter inference, Bioinformatics, Volume 35 (2019) no. 10, pp. 1720-1728 | DOI
[106] Reconstructing the macroevolutionary patterns of aphids (Hemiptera: Aphididae) using nuclear and mitochondrial DNA sequences, Biological Journal of the Linnean Society, Volume 121 (2017) no. 4, pp. 796-814 | DOI
[107] The R Project in Statistical Computing, MSOR Connections, Volume 1 (2001) no. 1, pp. 23-25 | DOI
[108] The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest, BMC Biology, Volume 18 (2020) no. 1 | DOI
[109] How important is intraspecific genetic admixture to the success of colonising populations?, Trends in Ecology & Evolution, Volume 29 (2014) no. 4, pp. 233-242 | DOI
[110] VSEARCH: a versatile open source tool for metagenomics, PeerJ, Volume 4 (2016) | DOI
[111] genepop’007: a complete re-implementation of the genepop software for Windows and Linux, Molecular Ecology Resources, Volume 8 (2008) no. 1, pp. 103-106 | DOI
[112] Inferring the mode of origin of polyploid species from next-generation sequence data, Molecular Ecology, Volume 24 (2015) no. 5, pp. 1047-1059 | DOI
[113] DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets, Molecular Biology and Evolution, Volume 34 (2017) no. 12, pp. 3299-3302 | DOI
[114] Uncovering symbiont-driven genetic diversity across North American pea aphids, Molecular Ecology, Volume 22 (2013) no. 7, pp. 2045-2059 | DOI
[115] Ecology and evolution of sex in aphids, Trends in Ecology & Evolution, Volume 17 (2002) no. 1, pp. 34-39 | DOI
[116] Evolutionary and functional insights into reproductive strategies of aphids, Comptes Rendus Biologies, Volume 333 (2010) no. 6-7, pp. 488-496 | DOI
[117] Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding, Scientific Reports, Volume 9 (2019) no. 1 | DOI
[118] Origins of the Apple: The Role of Megafaunal Mutualism in the Domestication of Malus and Rosaceous Trees, Frontiers in Plant Science, Volume 10 (2019) | DOI
[119] RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics, Volume 30 (2014) no. 9, pp. 1312-1313 | DOI
[120] Aphids of the genus Dysaphis Börner (Homoptera, Aphididae) living on plants of the family polygonaceae, Entomological Review, Volume 86 (2006) no. 7, pp. 787-805 | DOI
[121] The Role of Hybridization in the Evolution and Emergence of New Fungal Plant Pathogens, Phytopathology®, Volume 106 (2016) no. 2, pp. 104-112 | DOI
[122] The Origins of Plant Pathogens in Agro-Ecosystems, Annual Review of Phytopathology, Volume 46 (2008) no. 1, pp. 75-100 | DOI
[123] ADZE: a rarefaction approach for counting alleles private to combinations of populations, Bioinformatics, Volume 24 (2008) no. 21, pp. 2498-2504 | DOI
[124] Statistical method for testing the neutral mutation hypothesis by DNA polymorphism., Genetics, Volume 123 (1989) no. 3, pp. 585-595 | DOI
[125] Ethnobotany of the crab apple tree (Malus sylvestris (L.) Mill., Rosaceae) in Spain, Genetic Resources and Crop Evolution, Volume 68 (2021) no. 2, pp. 795-808 | DOI
[126] Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum, Molecular Ecology, Volume 11 (2002) no. 10, pp. 2123-2135 | DOI
[127] The eco-evolutionary impacts of domestication and agricultural practices on wild species, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 372 (2017) no. 1712 | DOI
[128] New insights from fine-scale spatial genetic structure analyses in plant populations, Molecular Ecology, Volume 13 (2004) no. 4, pp. 921-935 | DOI
[129] Environmentally related patterns of reproductive modes in the aphidMyzus persicaeand the predominance of two ‘superclones’ in Victoria, Australia, Molecular Ecology, Volume 12 (2003) no. 12, pp. 3493-3504 | DOI
[130] High Spatial Genetic Structure and Genetic Diversity in Chinese Populations ofSitobion miscanthi(Hemiptera: Aphididae), Journal of Economic Entomology, Volume 109 (2015) no. 1, pp. 375-384 | DOI
[131] Acibenzolar-S-Methyl Reprograms Apple Transcriptome Toward Resistance to Rosy Apple Aphid, Frontiers in Plant Science, Volume 9 (2018) | DOI
[132] On the number of segregating sites in genetical models without recombination, Theoretical Population Biology, Volume 7 (1975) no. 2, pp. 256-276 | DOI
[133] The homozygosity test of neutrality, Genetics, Volume 88 (1978) no. 2, pp. 405-417 | DOI
[134] ABCtoolbox: a versatile toolkit for approximate Bayesian computations, BMC Bioinformatics, Volume 11 (2010) no. 1 | DOI
[135] Migration and population genetics of the grain aphid Macrosiphum miscanti (Takahashi) in relation to the geographic distance and gene flow*, Progress in Natural Science, Volume 15 (2005) no. 11, pp. 1000-1004 | DOI
[136] Estimating F-Statistics for the Analysis of Population Structure, Evolution, Volume 38 (1984) no. 6 | DOI
[137] The influence of feeding of the rosy apple aphid, Dysaphis plantaginea (Pass.) (Homoptera: Aphididae) on the growth of apple fruits, . Roczniki Nauk Rolniczych. Seria E, Ochrona Roślin, Volume 23 (1993)
[138] Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication, Molecular Biology and Evolution, Volume 34 (2017) | DOI
[139] The invasion route for an insect pest species: the tobacco aphid in the New World, Molecular Ecology, Volume 19 (2010) no. 21, pp. 4738-4752 | DOI
[140] Low bacterial community diversity in two introduced aphid pests revealed with 16S rRNA amplicon sequencing, PeerJ, Volume 6 (2018) | DOI
[141] A multi-genome analysis approach enables tracking of the invasion of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World, Molecular Ecology, Volume 23 (2014) no. 8, pp. 1940-1951 | DOI
[142] Invasion Genetics of Woolly Apple Aphid (Hemiptera: Aphididae) in China, Journal of Economic Entomology, Volume 108 (2015) no. 3, pp. 1040-1046 | DOI
[143] The natural occurrence of secondary bacterial symbionts in aphids, Ecological Entomology, Volume 41 (2015) no. 1, pp. 13-26 | DOI
Cited by Sources: