{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T11:48:44Z","timestamp":1753876124254,"version":"3.41.2"},"reference-count":51,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2019,10,23]],"date-time":"2019-10-23T00:00:00Z","timestamp":1571788800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"National Key R&D Program of China","award":["2016YFE0203100"],"award-info":[{"award-number":["2016YFE0203100"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31620103916","31430078"],"award-info":[{"award-number":["31620103916","31430078"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Second Tibetan Plateau Scientific Expedition and Research","award":["QZKK0501"],"award-info":[{"award-number":["QZKK0501"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Wolbachia pipientis (Rickettsiales: Anaplasmataceae) is an intracellular symbiont residing in arthropods and filarial nematodes. Sixteen supergroups have been described from different host taxa. Four supergroups A, B, M, and N were found in aphids according to prior studies. The cotton aphid, Aphis gossypii, and the green peach aphid, Myzus persicae, are typical polyphagous species with global distributions. We conducted an extensive and systematic survey of Wolbachia infections in these aphids from China. High incidences of Wolbachia infection were detected. The total infection incidence was 60% in A. gossypii and 88% in M. persicae. Both aphid species were infected with supergroups A, B and M. Different incidences of infection were observed among the seven geographical regions in China, which suggested a positive relationship between Wolbachia infections and the geographical distribution of aphid species. Furthermore, multiple infection patterns (M, B, A&amp;M, B&amp;M, and A&amp;B&amp;M) were observed. Infection patterns M and B&amp;M were detected in almost all populations. Patterns A&amp;B&amp;M and B showed geographical restriction in North China. Three factors can possibly influence the Wolbachia infection incidences and patterns: the geographical distribution, aphid species, and different supergroup types.<\/jats:p>","DOI":"10.1093\/ee\/nvz122","type":"journal-article","created":{"date-parts":[[2019,10,8]],"date-time":"2019-10-08T08:12:33Z","timestamp":1570522353000},"source":"Crossref","is-referenced-by-count":1,"title":["Wolbachia Infection in Two Species: Novel Views on the Colonization Ability of Wolbachia in Aphids"],"prefix":"10.1093","author":[{"given":"Rui","family":"Chen","sequence":"first","affiliation":[{"name":"Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaomin","family":"Su","sequence":"additional","affiliation":[{"name":"Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jing","family":"Chen","sequence":"additional","affiliation":[{"name":"Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liyun","family":"Jiang","sequence":"additional","affiliation":[{"name":"Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ge-Xia","family":"Qiao","sequence":"additional","affiliation":[{"name":"Institute of Zoology, Chinese Academy of Sciences, Chaoyang District, Beijing, P.R. China"},{"name":"College of Life Sciences, University of the Chinese Academy of Sciences, Shijingshan District, Beijing, P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2019,10,23]]},"reference":[{"issue":"2","key":"2019102314531065100_CIT0001","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/een.12002","article-title":"Consistently high incidence of Wolbachia in global fig wasp communities","volume":"38","author":"Ahmed","year":"2013","journal-title":"Ecol. Entomol"},{"key":"2019102314531065100_CIT0002","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s12983-015-0107-z","article-title":"Wolbachia in butterflies and moths: geographic structure in infection frequency","volume":"12","author":"Ahmed","year":"2015","journal-title":"Front. Zool"},{"key":"2019102314531065100_CIT0003","doi-asserted-by":"crossref","first-page":"e28695","DOI":"10.1371\/journal.pone.0028695","article-title":"Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled?","volume":"6","author":"Augustinos","year":"2011","journal-title":"Plos One"},{"key":"2019102314531065100_CIT0004","doi-asserted-by":"crossref","first-page":"e112795","DOI":"10.1371\/journal.pone.0112795","article-title":"Wolbachia infections and mitochondrial diversity of two chestnut feeding Cydia species","volume":"9","author":"Avtzis","year":"2014","journal-title":"Plos One"},{"key":"2019102314531065100_CIT0005","volume-title":"Aphids on the word\u2019s crops. An identification and information guide","author":"Blackman","year":"2000","edition":"2nd ed"},{"key":"2019102314531065100_CIT0006","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/s00284-005-0084-0","article-title":"Discovery of a novel Wolbachia super group in Isoptera","volume":"51","author":"Bordenstein","year":"2005","journal-title":"Curr. Microbiol"},{"key":"2019102314531065100_CIT0007","first-page":"225","article-title":"Insect pest control using Wolbachia and\/or radiation,","volume-title":"K. Bourtzis and T. A. Miller (eds.), Insect Symbiosis, Vol. 2","author":"Bourtzis","year":"2006"},{"key":"2019102314531065100_CIT0008","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1099\/vir.0.012856-0","article-title":"Transcriptomic analysis of intestinal genes following acquisition of pea enation mosaic virus by the pea aphid Acyrthosiphon pisum","volume":"91","author":"Brault","year":"2010","journal-title":"J. Gen. Virol"},{"key":"2019102314531065100_CIT0009","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.ijpara.2003.10.004","article-title":"Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution","volume":"34","author":"Casiraghi","year":"2004","journal-title":"Int. J. Parasitol"},{"key":"2019102314531065100_CIT0010","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/1741-7007-6-27","article-title":"The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone","volume":"6","author":"Duron","year":"2008","journal-title":"BMC Biol"},{"key":"2019102314531065100_CIT0011","first-page":"47","article-title":"Arlequin (version 3.0): an integrated software package for population genetics data analysis","volume":"1","author":"Excoffier","year":"2007","journal-title":"Evol. Bioinform. Online"},{"key":"2019102314531065100_CIT0012","first-page":"294","article-title":"DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates","volume":"3","author":"Folmer","year":"1994","journal-title":"Mol. March Biol. Biotechnol"},{"key":"2019102314531065100_CIT0013","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.meegid.2014.12.019","article-title":"New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae)","volume":"30","author":"Glowska","year":"2015","journal-title":"Infect. Genet. Evol"},{"key":"2019102314531065100_CIT0014","doi-asserted-by":"crossref","first-page":"6626","DOI":"10.1128\/JB.186.19.6626-6633.2004","article-title":"Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri","volume":"186","author":"G\u00f3mez-Valero","year":"2004","journal-title":"J. Bacteriol"},{"key":"2019102314531065100_CIT0015","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1645\/0022-3395(2003)089[0283:WEIFS]2.0.CO;2","article-title":"Wolbachia endosymbionts in fleas (Siphonaptera)","volume":"89","author":"Gorham","year":"2003","journal-title":"J. Parasitol"},{"key":"2019102314531065100_CIT0016","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1016\/j.ijpara.2009.01.006","article-title":"An endosymbiotic bacterium in a plant-parasitic nematode: member of a new Wolbachia supergroup","volume":"39","author":"Haegeman","year":"2009","journal-title":"Int. J. Parasitol"},{"key":"2019102314531065100_CIT0017","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1111\/j.1574-6968.2008.01110.x","article-title":"How many species are infected with Wolbachia? A statistical analysis of current data","volume":"281","author":"Hilgenboecker","year":"2008","journal-title":"FEMS Microbiol. Lett"},{"key":"2019102314531065100_CIT0019","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.meegid.2014.07.026","article-title":"Wolbachia infection status and genetic structure in natural populations of Polytremis nascens (Lepidoptera: Hesperiidae)","volume":"27","author":"Jiang","year":"2014","journal-title":"Infect. Genet. Evol"},{"key":"2019102314531065100_CIT0020","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.molbiopara.2008.04.012","article-title":"Molecular identification of Wolbachia from the filarial nematode Mansonella perstans","volume":"160","author":"Keiser","year":"2008","journal-title":"Mol. Biochem. Parasitol"},{"key":"2019102314531065100_CIT0021","doi-asserted-by":"crossref","first-page":"2405","DOI":"10.1111\/j.1365-294X.2004.02213.x","article-title":"Reproductive effects and geographical distributions of two Wolbachia strains infecting the Neotropical beetle, Chelymorpha alternans Boh. (Chrysomelidae, Cassidinae)","volume":"13","author":"Keller","year":"2004","journal-title":"Mol. Ecol"},{"key":"2019102314531065100_CIT0022","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1046\/j.0962-1083.2001.01432.x","article-title":"Prevailing triple infection with Wolbachia in Callosobruchus chinensis (Coleoptera: Bruchidae)","volume":"11","author":"Kondo","year":"2002","journal-title":"Mol. Ecol"},{"key":"2019102314531065100_CIT0023","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1093\/bioinformatics\/btp187","article-title":"DnaSP v5: a software for comprehensive analysis of DNA polymorphism data","volume":"25","author":"Librado","year":"2009","journal-title":"Bioinformatics"},{"key":"2019102314531065100_CIT0024","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/j.jip.2012.01.001","article-title":"Presence and distribution of the endosymbiont Wolbachia among Solenopsis spp. (Hymenoptera: Formicidae) from Brazil and its evolutionary history","volume":"109","author":"Martins","year":"2012","journal-title":"J. Invertebr. Pathol"},{"key":"2019102314531065100_CIT0025","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1017\/S0007485315000085","article-title":"Broader prevalence of Wolbachia in insects including potential human disease vectors","volume":"105","author":"de Oliveira","year":"2015","journal-title":"Bull. Entomol. Res"},{"key":"2019102314531065100_CIT0026","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1146\/annurev-ento-112408-085305","article-title":"Facultative symbionts in aphids and the horizontal transfer of ecologically important traits","volume":"55","author":"Oliver","year":"2010","journal-title":"Annu. Rev. Entomol"},{"key":"2019102314531065100_CIT0027","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1093\/molbev\/msn083","article-title":"jModelTest: phylogenetic model averaging","volume":"25","author":"Posada","year":"2008","journal-title":"Mol. Biol. Evol"},{"key":"2019102314531065100_CIT0028","first-page":"198","article-title":"Diversity and geographical distributions of Wolbachia infecting the endoparasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae) in China","volume":"4","author":"Qi","year":"2016","journal-title":"Acad. J. Agricull. Res"},{"key":"2019102314531065100_CIT0029","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1111\/j.1558-5646.2008.00533.x","article-title":"Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgression, and codivergence in the Nasonia species complex","volume":"63","author":"Raychoudhury","year":"2009","journal-title":"Evolution"},{"key":"2019102314531065100_CIT0030","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1007\/0-387-30745-1_22","article-title":"The genus Wolbachia","volume":"5","author":"Riegler","year":"2006","journal-title":"Prokayotes"},{"key":"2019102314531065100_CIT0031","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1093\/ee\/27.2.337","article-title":"Predicting phenology of green peach aphid using degree-days","volume":"27","author":"Ro","year":"1998","journal-title":"Environ. Entomol"},{"key":"2019102314531065100_CIT0032","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1093\/sysbio\/sys029","article-title":"MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space","volume":"61","author":"Ronquist","year":"2012","journal-title":"Syst. Biol"},{"key":"2019102314531065100_CIT0033","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.1128\/AEM.01109-08","article-title":"How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae)","volume":"75","author":"Ros","year":"2009","journal-title":"Appl. Environ. Microbiol"},{"key":"2019102314531065100_CIT0034","doi-asserted-by":"crossref","first-page":"3161","DOI":"10.1128\/AEM.72.5.3161-3167.2006","article-title":"Wolbachia infections in the Cimicidae: museum specimens as an untapped resource for endosymbiont surveys","volume":"72","author":"Sakamoto","year":"2006","journal-title":"Appl. Environ. Microbiol"},{"key":"2019102314531065100_CIT0035","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.mib.2009.11.005","article-title":"Wolbachia: more than just a bug in insects genitals","volume":"13","author":"Saridaki","year":"2010","journal-title":"Curr. Opin. Microbiol"},{"key":"2019102314531065100_CIT0037","doi-asserted-by":"crossref","first-page":"7537","DOI":"10.1128\/AEM.01541-09","article-title":"Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities","volume":"75","author":"Schloss","year":"2009","journal-title":"Appl. Environ. Microbiol"},{"key":"2019102314531065100_CIT0038","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1111\/j.1755-0998.2010.02955.x","article-title":"Wolbachia detection: an assessment of standard PCR protocols","volume":"11","author":"Sim\u00f5es","year":"2011","journal-title":"Mol. Ecol. Resour"},{"key":"2019102314531065100_CIT0039","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1080\/10635150802429642","article-title":"A rapid bootstrap algorithm for the RAxML Web servers","volume":"57","author":"Stamatakis","year":"2008","journal-title":"Syst. Biol"},{"key":"2019102314531065100_CIT0040","doi-asserted-by":"crossref","first-page":"2725","DOI":"10.1093\/molbev\/mst197","article-title":"MEGA6: Molecular Evolutionary Genetics Analysis version 6.0","volume":"30","author":"Tamura","year":"2013","journal-title":"Mol. Biol. Evol"},{"key":"2019102314531065100_CIT0041","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1007\/s00284-002-4010-4","article-title":"Molecular evidence of Wolbachia infection in natural populations of tropical odonates","volume":"47","author":"Thipaksorn","year":"2003","journal-title":"Curr. Microbiol"},{"key":"2019102314531065100_CIT0042","first-page":"1823","article-title":"Current research trends on the endosymbiont Wolbachia in insects","volume":"48","author":"Wang","year":"2011","journal-title":"J. Appl. Entomol"},{"key":"2019102314531065100_CIT0043","doi-asserted-by":"crossref","first-page":"49","DOI":"10.14411\/eje.2009.007","article-title":"Distribution and diversity of Wolbachia in different populations of the wheat aphid Sitobion miscanthi (Hemiptera: Aphididae) in China","volume":"106","author":"Wang","year":"2009","journal-title":"Eur. J. Entomol"},{"key":"2019102314531065100_CIT0044","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1111\/1744-7917.12102","article-title":"Widespread infection and diverse infection patterns of Wolbachia in Chinese aphids","volume":"21","author":"Wang","year":"2014","journal-title":"Insect Sci"},{"key":"2019102314531065100_CIT0045","doi-asserted-by":"crossref","first-page":"20150249","DOI":"10.1098\/rspb.2015.0249","article-title":"The incidence of bacterial endosymbionts in terrestrial arthropods","volume":"282","author":"Weinert","year":"2015","journal-title":"Proc. Biol. Sci"},{"key":"2019102314531065100_CIT0046","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1098\/rspb.1998.0456","article-title":"Widespread occurrence of the micro-organism Wolbachia in ants","volume":"265","author":"Wenseleers","year":"1998","journal-title":"Proc. Biol. Sci"},{"key":"2019102314531065100_CIT0047","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1146\/annurev.ento.42.1.587","article-title":"Biology of Wolbachia","volume":"42","author":"Werren","year":"1997","journal-title":"Annu. Rev. Entomol"},{"key":"2019102314531065100_CIT0048","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1098\/rspb.2000.1139","article-title":"Wolbachia infection frequencies in insects: evidence of a global equilibrium?","volume":"267","author":"Werren","year":"2000","journal-title":"Proc. Biol. Sci"},{"key":"2019102314531065100_CIT0049","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/nrmicro1969","article-title":"Wolbachia: master manipulators of invertebrate biology","volume":"6","author":"Werren","year":"2008","journal-title":"Nat. Rev. Microbiol"},{"key":"2019102314531065100_CIT0050","first-page":"387","volume-title":"Economic insect fauna of China Fasc. 25 Homoptera: Aphidinea, part I","author":"Zhang","year":"1983"},{"key":"2019102314531065100_CIT0051","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1098\/rspb.1998.0324","article-title":"Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences","volume":"265","author":"Zhou","year":"1998","journal-title":"Proc. Biol. Sci"},{"issue":"6","key":"2019102314531065100_CIT0052","doi-asserted-by":"crossref","first-page":"e02546-17","DOI":"10.1128\/AEM.02546-17","article-title":"Incidence of facultative bacterial endosymbionts in spider mites associated with local environments and host plants","volume":"84","author":"Zhu","year":"2018","journal-title":"Appl. Environ. Microbiol"},{"key":"2019102314531065100_CIT0053","doi-asserted-by":"crossref","first-page":"e38544","DOI":"10.1371\/journal.pone.0038544","article-title":"Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected","volume":"7","author":"Zug","year":"2012","journal-title":"Plos One"}],"container-title":["Environmental Entomology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/ee\/advance-article-pdf\/doi\/10.1093\/ee\/nvz122\/30279097\/nvz122.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ee\/advance-article-pdf\/doi\/10.1093\/ee\/nvz122\/30279097\/nvz122.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,10,23]],"date-time":"2019-10-23T19:09:27Z","timestamp":1571857767000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ee\/advance-article\/doi\/10.1093\/ee\/nvz122\/5603787"}},"subtitle":[],"editor":[{"given":"Nick","family":"Miller","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2019,10,23]]},"references-count":51,"URL":"https:\/\/doi.org\/10.1093\/ee\/nvz122","relation":{},"ISSN":["0046-225X","1938-2936"],"issn-type":[{"type":"print","value":"0046-225X"},{"type":"electronic","value":"1938-2936"}],"subject":[],"published":{"date-parts":[[2019,10,23]]},"article-number":"nvz122"}}