Tracking the origin and dispersal of the Asian chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera, Cynipidae) in Europe with molecular markers.

The Asian chestnut gall wasp, Dryocosmus kuriphilus, is an invasive pest causing significant damage to chestnut trees (Castanea spp., Fagaceae). Originating from China, it has recently invaded a wide range of regions in Europe and North America. Understanding the population genetic structure of important invasive pests is very useful for improving the knowledge concerning routes of expansion and colonizing capacity. Despite its economic importance, limited attention has been given to D. kuriphilus origin and spread, or to its genetic structure. In this study, D. kuriphilus populations sampled in eight European countries were screened using both mitochondrial (cytochrome c oxidase subunit 1; COI) and nuclear (internal transcribed spacer 2; ITS2) sequences, and Amplified Fragment Length Polymorphism (AFLP) markers. The molecular markers COI and ITS2 highlighted the presence of a single haplotype in all the studied populations. The recorded mitochondrial haplotype was identical to one of the most widespread haplotypes occurring in the native area (China). AFLP results indicated that D. kuriphilus individuals belong to two genetically distinct clusters without any further geographic clustering. These results suggest that D. kuriphilus populations in Europe could be the result of a single introduction of a Chinese founder population characterized by two genetically distinct lineages that subsequently spread rapidly across Europe. However, the possibility that populations originated from multiple introductions of the same Chinese mitochondrial haplotype cannot be excluded. The reported results provide useful information concerning this invasive species, potentially facilitating integrated pest management.

[1]  M. Faccoli,et al.  Do Torymus sinensis (Hymenoptera: Torymidae) and agroforestry system affect native parasitoids associated with the Asian chestnut gall wasp? , 2018, Biological Control.

[2]  S. Vezzulli,et al.  Genetic variability in Italian populations of Drosophila suzukii , 2017, BMC Genetics.

[3]  Y. Gninenko,et al.  East chestnut gall wasps Dryocosmus kuriphilus Yasumatsu, 1951 (Hymenoptera, Cynipidae)—New invader in the forests of the North Caucasus , 2017, Russian Journal of Biological Invasions.

[4]  J. Kollár,et al.  Occurrence of oriental chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera, Cynipidae) in Slovakia – short communication , 2017 .

[5]  A. F. van den Hurk,et al.  Tiger on the prowl: Invasion history and spatio-temporal genetic structure of the Asian tiger mosquito Aedes albopictus (Skuse 1894) in the Indo-Pacific , 2017, PLoS neglected tropical diseases.

[6]  R. F. Medina,et al.  Genetic population structure of sugarcane aphid, Melanaphis sacchari, in sorghum, sugarcane, and Johnsongrass in the continental USA , 2017 .

[7]  F. Scolari,et al.  Genetic evidence for a worldwide chaotic dispersion pattern of the arbovirus vector, Aedes albopictus , 2017, PLoS neglected tropical diseases.

[8]  D. Papachristos,et al.  First record of Dryocosmus kuriphilus in Greece , 2016 .

[9]  F. Colombari,et al.  Native and introduced parasitoids in the biocontrol of Dryocosmus kuriphilus in Veneto (Italy) , 2016 .

[10]  F. Zalom,et al.  Microsatellite Variation of two Pacific Coast Drosophila suzukii (Diptera: Drosophilidae) Populations , 2015, Environmental entomology.

[11]  G. Zúñiga,et al.  Phenotypic and Genetic Variations in Obligate Parthenogenetic Populations of Eriosoma lanigerum Hausmann (Hemiptera: Aphididae) , 2015, Neotropical Entomology.

[12]  M. Navajas,et al.  Genetic traits leading to invasion: plasticity in cold hardiness explains current distribution of an invasive agricultural pest, Tetranychus evansi (Acari: Tetranychidae) , 2015, Biological Invasions.

[13]  Andrea Battisti,et al.  Invasion by the chestnut gall wasp in Italy causes significant yield loss in Castanea sativa nut production , 2014 .

[14]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[15]  R. Montiel,et al.  Living on a volcano’s edge: genetic isolation of an extremophile terrestrial metazoan , 2013, Heredity.

[16]  D. Avtzis,et al.  Taking Europe by storm: a first insight in the introduction and expansion of Dryocosmus kuriphilus in central Europe by mtDNA. , 2013 .

[17]  Christopher Phillips,et al.  An overview of STRUCTURE: applications, parameter settings, and supporting software , 2013, Front. Genet..

[18]  K. Schönrogge,et al.  Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic. , 2013, Zootaxa.

[19]  A. Alma,et al.  Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north‐western Italy , 2013 .

[20]  E. Guerrieri,et al.  Biology and monitoring of Dryocosmus kuriphilus on Castanea sativa in Southern Italy , 2013 .

[21]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[22]  Richard J. Challis,et al.  Mitochondrial barcodes are diagnostic of shared refugia but not species in hybridizing oak gallwasps , 2012, Molecular ecology.

[23]  B. Jordal,et al.  Improbable but true: the invasive inbreeding ambrosia beetle Xylosandrus morigerus has generalist genotypes , 2012, Ecology and evolution.

[24]  E. Scholte,et al.  Aedes aegypti Mosquitoes Imported into the Netherlands, 2010 , 2011, Emerging infectious diseases.

[25]  N. Bennett,et al.  Low levels of polymorphism at novel microsatellite loci developed for bathyergid mole-rats from South Africa , 2011, Conservation Genetics Resources.

[26]  R. Brandl,et al.  No host‐associated differentiation in the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae) on three dog rose species , 2011 .

[27]  D. Matošević Oriental chestnut gall wasp (Dryocosmus kuriphilus) in Croatia. , 2010 .

[28]  M. Kolšek,et al.  Experience with Dryocosmus kuriphilus Yasumatsu eradication measures in Slovenia , 2010 .

[29]  M. Ciomperlik,et al.  Development of a Ribosomal DNA ITS2 Marker for the Identification of the Thrips, Scirtothrips dorsalis , 2010, Journal of insect science.

[30]  P. Hulme Trade, transport and trouble: managing invasive species pathways in an era of globalization , 2009 .

[31]  A. Alma,et al.  Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus , 2008, BioControl.

[32]  R. Butlin,et al.  An objective, rapid and reproducible method for scoring AFLP peak‐height data that minimizes genotyping error , 2008, Molecular ecology resources.

[33]  C. Zebitz,et al.  Genetic divergence of Trichogramma aurosum Sugonjaev and Sorokina (Hymenoptera: Trichogrammatidae) individuals based on ITS2 and AFLP analysis , 2008 .

[34]  A. Forneck,et al.  Analysis of genetic variation within clonal lineages of grape phylloxera (Daktulosphaira vitifoliae Fitch) using AFLP fingerprinting and DNA sequencing. , 2007, Genome.

[35]  G. Stone,et al.  The diversity and phylogeography of cynipid gallwasps (Hymenoptera: Cynipidae) of the Oriental and eastern Palearctic regions, and their associated communities , 2007 .

[36]  Z. Pénzes,et al.  The phylogenetic relationships between Dryocosmus, Chilaspis and allied genera of oak gallwasps (Hymenoptera, Cynipidae: Cynipini) , 2007 .

[37]  M. Christman,et al.  Number of individuals and molecular markers to use in genetic differentiation studies , 2006 .

[38]  D. Ehrich aflpdat: a collection of r functions for convenient handling of AFLP data , 2006 .

[39]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[40]  J. Mappes,et al.  The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations , 2005, Molecular ecology.

[41]  P. Schönswetter,et al.  Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae) , 2005 .

[42]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[43]  A. Cognato,et al.  Genetic variation and origin of red turpentine beetle (Dendroctonus valens LeConte) introduced to the People's Republic of China , 2005 .

[44]  B. Zwaan,et al.  Genetic diversity and Wolbachia infection of the Drosophila parasitoid Leptopilina clavipes in western Europe , 2004, Molecular ecology.

[45]  J. Frydenberg,et al.  Genetic diversity and the phylogeography of parthenogenesis: comparing bisexual and thelytokous populations of Nemasoma varicorne (Diplopoda: Nemasomatidae) in Denmark. , 2002, Hereditas.

[46]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[47]  Matthew Stephens,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[48]  F. Sebastiani,et al.  Genetic aspects of the worldwide colonization process of Ceratitis capitata. , 1998, The Journal of heredity.

[49]  F. Collins,et al.  A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species , 1996, Insect molecular biology.

[50]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[51]  M. Lynch,et al.  Analysis of population genetic structure with RAPD markers , 1994, Molecular ecology.

[52]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[53]  K. Nohara,et al.  Considerations on the reproductive capacity of Dryocosmus kuriphilus Yasumatsu (Hymenoptera : Cynipidae) , 1956 .

[54]  Andrew M. Liebhold,et al.  Impact of Non-native Invertebrates and Pathogens on Market Forest Tree Resources , 2017 .

[55]  C. Malumphy First findings of oriental chestnut gael wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in the United Kingdom. , 2015 .

[56]  E. Orman,et al.  First record of the oriental chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in Turkey. , 2014 .

[57]  Dina M. Fonseca,et al.  Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys , 2013, Biological Invasions.

[58]  J. Aronson,et al.  Impacts of biological invasions: what's what and the way forward. , 2013, Trends in ecology & evolution.

[59]  Juli Pujade-Villar,et al.  Nota entomològica. Primeres troballes a la península Ibèrica de Dryocosmus kuriphilus (Hym., Cynipidae), una espècie de cinípid d’origen asiàtic altament perillosa per al castanyer (Fagaceae) , 2013 .

[60]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[61]  Lu Peng Phylogenetic analysis of the mtDNA COI gene suggests cryptic Dryocosmus kuriphilus associated with certain populations of Chinese chestnuts (Castanea spp.) , 2012 .

[62]  G. Csóka,et al.  The oriental sweet chestnut gall wasp (Dryocosmus kuriphilus Yasumatsu 1951) in Hungary. , 2009 .

[63]  F. Meier,et al.  Die Edelkastaniengallwespe Dryocosmus kuriphilus (Yasumatsu) (Hymenoptera, Cynipidae) tritt erstmals in der Südschweiz auf , 2009 .

[64]  K. Schönrogge,et al.  Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus , 2006 .

[65]  K. Yara Identification of Torymus sinensis and T. beneficus (Hymenoptera: Torymidae), introduced and indigenous parasitoids of the chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae), using the ribosomal ITS2 region , 2006 .

[66]  A. Clarke,et al.  Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. , 2005, Annual review of entomology.

[67]  G. Brussino Pericoloso insetto esotico per il castagno europeo , 2002 .

[68]  P. Vos,et al.  AFLP: a new technique for DNA fingerprinting. , 1995, Nucleic acids research.

[69]  Yosiaki Itǒ,et al.  Population Dynamics of the Chestnut Gall-wasp Dryocosmus kuriphilus YASUMATSU (Hymenoptera: Cynipidae) , 1964 .