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Co-haplotyping symbiont and host to unravel invasion pathways of the exotic pest Halyomorpha halys in Italy

  • 1.

    Lashkari, M. et al. Global genetic variation in the Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae) and the endosymbiont Wolbachia: links between Iran and the USA detected. Pest Manag. Sci. 70, 1033–1040 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 2.

    Wang, Y. et al. Phylogeography of Diaphorina citri (Hemiptera: Liviidae) and its primary endosymbiont, ‘Candidatus Carsonella ruddii’: An evolutionary approach to host–endosymbiont interaction. Pest Manag. Sci. 74, 2185–2194 (2018).

    CAS  Article  Google Scholar 

  • 3.

    Otero-Bravo, A. & Sabree, Z. L. Comparing the utility of host and primary endosymbiont loci for predicting global invasive insect genetic structuring and migration patterns. Biol. Control. 116, 1016 (2018).

    Article  Google Scholar 

  • 4.

    Savio, C. et al. Evidence of two lineages of the symbiont ‘Candidatus Erwinia dacicola’ in Italian populations of Bactrocera oleae (Rossi) based on 16S rRNA gene sequences. Int. J. Syst. Evol. Micr. 62, 179–187 (2012).

    CAS  Article  Google Scholar 

  • 5.

    Funk, D. J., Helbling, L., Wernegreen, J. J. & Moran, N. A. Intraspecific phylogenetic congruence among multiple symbiont genomes. P. Roy Soc. B-Biol. Sci. 267, 2517–2521 (2000).

    CAS  Article  Google Scholar 

  • 6.

    Criscione, C. D., Cooper, B. & Blouin, M. S. Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87, 823–828 (2006).

    PubMed  Article  Google Scholar 

  • 7.

    Brown, J. E. et al. Aedes aegypti mosquitoes imported into the Netherlands, 2010. Emerg. Infect. Dis. 17, 2335 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  • 8.

    Simberloff, D. et al. Impacts of biological invasions: What’s what and the way forward. Trends Ecol. Evol. 28, 58–66 (2013).

    PubMed  Article  Google Scholar 

  • 9.

    Maynard, A. J. 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. PLoS Neglect. Trop. D. 11, e0005546 (2017).

    Article  Google Scholar 

  • 10.

    Bansal, R., Michel, A. & Sabree, Z. The crypt-dwelling primary bacterial symbiont of the polyphagous pentatomid pest Halyomorpha halys (Hemiptera: Pentatomidae). Environ. Entomol. 43, 617–625 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Kenyon, L. J., Meulia, T. & Sabree, Z. L. Habitat visualization and genomic analysis of “Candidatus Pantoea carbekii”, the primary symbiont of the brown marmorated stink bug. Genome Biol. Evol. 7, 620–635 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 12.

    Leskey, T. C. & Nielsen, A. L. Impact of the invasive brown marmorated stink bug in North America and Europe: History, biology, ecology, and management. Annu. Rev. Entomol. 63, 599–618 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 13.

    Moore, L. et al. Characterizing damage potential of the brown marmorated stink bug in cherry orchards in Italy. Entomol. Gen. 3–4, 271–283 (2019).

    Article  Google Scholar 

  • 14.

    Rice, K. B. et al. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J. Integr. Pest Manag. 5, 1–13 (2014).

    Article  Google Scholar 

  • 15.

    Wermelinger, B., Wyniger, D. & Forster, B. First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees?. Mitt. Schweiz. Entomol. Ges. 81, 1–8 (2008).

    Google Scholar 

  • 16.

    Arnold, K. Halyomorpha halys (Stål, 1855), Eine fur die europaische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt. Thür. Entomologogenverbande. 16, 19 (2009).

    Google Scholar 

  • 17.

    Heckmann, R. Erster nachweis von Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) für deutschland. Heteropteron 36, 17–18 (2012).

    Google Scholar 

  • 18.

    Callot, H. & Brua, C. Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espece pour la faune de France (Heteroptera Pentatomidae). Entomologiste. 69, 69–71 (2013).

    Google Scholar 

  • 19.

    Maistrello, L. et al. First records in Italy of the Asian stinkbug Halyomorpha halys a new threat to fruit crops. Atti Giornate Fitopatologiche. 1, 283–288 (2014).

    Google Scholar 

  • 20.

    Gariepy, T. D., Haye, T., Fraser, H. & Zhang, J. Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J. Pest Sci. 87, 17–28 (2014).

    Article  Google Scholar 

  • 21.

    Milonas, P. G. & Partsinevelos, G. K. First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull. 44, 183–186 (2014).

    Article  Google Scholar 

  • 22.

    Vétek, G., Papp, V., Haltrich, A. & Rédei, D. First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa. 3780, 194–200 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 23.

    Cesari, M. et al. A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J. Pest Sci. 88, 1–7 (2015).

    Article  Google Scholar 

  • 24.

    Macavei, L. et al. First detection of Halyomorpha halys, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucr. Stiint. Ser. Agron. 58, 105–108 (2015).

    Google Scholar 

  • 25.

    Rabitsch, W. & Griebe, G. J. From the west and from the east? First records of Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae) in Vorarlberg and Vienna, Austria. Beitr. Entomof. 16, 115–139 (2015).

    Google Scholar 

  • 26.

    Šeat, J. Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomol. Serbica. 20, 167–171 (2015).

    Google Scholar 

  • 27.

    Maurel, J. P., Blaye, G., Valladares, L., Roinel, É. & Cochard, P. O. Halyomorpha halys (Stål, 1855), la punaise diabolique en France, a Toulouse (Heteroptera; Pentatomidae). Carnets Nat. 3, 2125 (2016).

    Google Scholar 

  • 28.

    Dioli, P., Leo, P. & Maistrello, L. Prime segnalazioni in Spagna e in Sardegna della specie aliena Halyomorpha halys (Stål, 1855) e note sulla sua distribuzione in Europa (Hemiptera, Pentatomidae). Rev. gaditana Entomol. 7, 539–548 (2016).

    Google Scholar 

  • 29.

    Simov, N. The invasive brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) already in Bulgaria. Ecol. Montenegrina. 9, 51–53 (2016).

    Article  Google Scholar 

  • 30.

    Hemala, V. & Kment, P. First record of Halyomorpha halys and mass occurrence of Nezara viridula in Slovakia. Plant Prot. Sci. 53, 1–7 (2017).

    Article  Google Scholar 

  • 31.

    Claerebout, S., Haye, T., Olafsson, E., Pannier, E. & Bultot, J. Premières occurrences de Halyomorpha halys (Stål, 1855) pour la Belgique et actualisation de sa répartition en Europe (Hemiptera: Heteroptera: Pentatomidae). Bull. Soc. R. belge entomolog. 154, 205–227 (2019).

    Google Scholar 

  • 32.

    Tassini, C. & Mifsud, D. The brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae) in Malta. EPPO Bull. 49, 132–136 (2019).

    Article  Google Scholar 

  • 33.

    Zovko, M., Ostojić, I., Jurković, D., & Karić, N. (2019). First report of the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) in Bosnia and Herzegovina. Radovi Poljoprivredno Prehrambenog Fakulteta Univerziteta u SarajevuWorks of the Faculty of Agricultural and Food Sciences University of Sarajevo. 64, 68–78 (2019).

  • 34.

    Gapon, D. A. First records of the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Georgia. Entomol. Rev. 96, 1086–1088 (2016).

    Article  Google Scholar 

  • 35.

    Musolin, D. L. et al. Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops. Arthropod.-Plant Interact. 12, 517–529 (2018).

    Article  Google Scholar 

  • 36.

    Kriticos, D. J. The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J. Pest Sci. 90, 1033–1043 (2017).

    Article  Google Scholar 

  • 37.

    Kapantaidaki, D. E. et al. Halyomorpha halys (Hemiptera: Pentatomidae) genetic diversity in North America and Europe. Insects 10, 174. https://doi.org/10.3390/insects10060174 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  • 38.

    Xu, J., Fonseca, D. M., Hamilton, G. C., Hoelmer, K. A. & Nielsen, A. L. Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol. Invas. 16, 153–166 (2014).

    CAS  Article  Google Scholar 

  • 39.

    Cesari, M. et al. Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy. Biol. Invas. 20, 1073–1092 (2018).

    Article  Google Scholar 

  • 40.

    Zhu, G. P. et al. Range wide molecular data and niche modeling revealed the Pleistocene history of a global invader (Halyomorpha halys). Sci. Rep. 6, 23192 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 41.

    Valentin, R. E., Nielsen, A. L., Wiman, N. G., Lee, D. H. & Fonseca, D. M. Global invasion network of the brown marmorated stink bug, Halyomorpha halys. Sci. Rep. 7, 9866 (2017).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Lee, W. et al. Genetic diversity of Halyomorpha halys (Hemiptera, Pentatomidae) in South Korea and comparison with COI sequence datasets from East Asia, Europe, and North America. Fla. Entomol. 101, 49–55 (2018).

    Article  Google Scholar 

  • 43.

    Morrison, W. R. et al. Attraction of Halyomorpha halys (Hemiptera: Pentatomidae) haplotypes in North America and Europe to baited traps. Sci. Rep. 7, 16941. https://doi.org/10.1038/s41598-017-17233-0 (2017).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 44.

    Dlugosch, K. M. & Parker, I. M. Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431–449 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Freers, A. Blinde Passagiere: Stinkwanzen, Marmorierte Baumwanze—Halyomorpha halys. https://ssl.bremen.de/lmtvet/sixcms/media.php/13/Blinde_Passagiere_Stinkwanze_3_2012.pdf. (2012).

  • 46.

    Gariepy, T. D., Bruin, A., Haye, T., Milonas, P. & Vétek, G. Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe. J. Pest Sci. 88, 451–460 (2015).

    Article  Google Scholar 

  • 47.

    Croteau, E. K. Causes and consequences of dispersal in plants and animals. Nat. Educ. Know. 3, 12 (2010).

    Google Scholar 

  • 48.

    Schellhorn, N. A., Bianchi, F. J. J. A. & Hsu, C. L. Movement of entomophagous arthropods in agricultural landscapes: Links to pest suppression. Annu. Rev. Entomol. 59, 559–581 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 49.

    Rassati, D., Faccoli, M., Petrucco Toffolo, E., Battisti, A. & Marini, L. Improving the early detection of alien wood-boring beetles in ports and surrounding forests. J. Appl. Ecol. 52, 50–58 (2015).

    CAS  Article  Google Scholar 

  • 50.

    Duthie, C., Michael, T., Stephenson, B., Yamoah, E. & McDonald, B. Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways (Ministry for Primary Industries, Wellington, 2012).

    Google Scholar 

  • 51.

    Haye, T. et al. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J. Pest Sci. 88, 665–673 (2015).

    Article  Google Scholar 

  • 52.

    Vandervoet, T. F., Bellamy, D. E., Anderson, D. & MacLellan, R. Trapping for early detection of the brown marmorated stink bug, Halyomorpha halys, New Zealand. N. Z. Plant Prot. 72, 36–43 (2019).

    Google Scholar 

  • 53.

    Hosokawa, T., Matsuura, Y., Kikuchi, Y. & Fukatsu, T. Recurrent evolution of gut symbiotic bacteria in pentatomid stinkbugs. Zool. Let. 2, 24 (2016).

    Article  Google Scholar 

  • 54.

    Allen, J. M., Light, J. E., Perotti, M. A., Braig, H. R. & Reed, D. L. Mutational meltdown in primary endosymbionts: Selection limits Muller’s ratchet. PLoS ONE 4, 2 (2009).

    Google Scholar 

  • 55.

    Perotti, M. A., Allen, J. M., Reed, D. L. & Braig, H. R. Host-symbiont interactions of the primary endosymbiont of human head and body lice. FASEB J. 21, 1058–1066 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 56.

    Ohbayashi, T. et al. Insect’s intestinal organ for symbiont sorting. Proc. Natl. Acad. Sci. USA 112, E5179–E5188 (2015).

    CAS  PubMed  Article  Google Scholar 

  • 57.

    Liu, Q. et al. A chromosomal-level genome assembly for the insect vector for Chagas disease, Triatoma rubrofasciata. GigaScience 8, 89 (2019).

    ADS  Article  CAS  Google Scholar 

  • 58.

    Maistrello, L., Dioli, P., Bariselli, M., Mazzoli, G. L. & Giacalone-Forini, I. Citizen science and early detection of invasive species: Phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol. Invas. 18, 3109–3116 (2016).

    Article  Google Scholar 

  • 59.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 60.

    Kearse, M. et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 61.

    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 62.

    Schloss, P. D., Delalibera, I., Handelsman, J. & Raffa, K. F. Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environ. Entomol. 35, 625–629 (2006).

    Article  Google Scholar 

  • 63.

    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 35: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 64.

    Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).

    Article  Google Scholar 

  • 65.

    Clement, M., Posada, D. & Crandall, K. A. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 66.

    Blüthgen, N., Menzel, F. & Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol. 6, 9 (2006).

    PubMed  PubMed Central  Article  Google Scholar 

  • 67.

    Dáttilo, W. Different tolerances of symbiotic and nonsymbiotic ant-plant networks to species extinctions. Netw. Biol. 2, 127 (2012).

    Google Scholar 

  • 68.

    Almeida-Neto, M., Guimaraes, P., Guimaraes, P. R. Jr., Loyola, R. D. & Ulrich, W. A consistent metric for nestedness analysis in ecological systems: Reconciling concept and measurement. Oikos 117, 1227–1239 (2008).

    Article  Google Scholar 

  • 69.

    Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: Analysing ecological networks. R news 8, 8–11 (2008).

    Google Scholar 

  • 70.

    Tillman, P. G., Greenstone, M. H. & Hu, J. S. Predation of stink bugs (Hemiptera: Pentatomidae) by a complex of predators in cotton and adjoining soybean habitats in Georgia, USA. Fla. Entomol. 2, 1114–1126 (2015).

    Article  Google Scholar 

  • 71.

    Šapina, I. & Jelaska, L. Š. First report of invasive brown marmorated stink bug Halyomorpha halys (Stål, 1855) in Croatia. EPPO Bull. 48, 138–143 (2018).

    Article  Google Scholar 

  • 72.

    Dhami, M. K., Dsouza, M., Waite, D. W., Anderson, D. & Li, D. Real-Time PCR assay for the identification of the Brown Marmorated Stink Bug (Halyomorpha halys). Front. Mol. Biosci. 3, 5 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 


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