Insectes Sociaux

, Volume 64, Issue 3, pp 313–320

The origin and genetic diversity of the yellow-legged hornet, Vespa velutina introduced in Japan

  • T. Takeuchi
  • R. Takahashi
  • T. Kiyoshi
  • M. Nakamura
  • Y. N. Minoshima
  • J. Takahashi
Research Article

Abstract

Biological invasions have severe economic and ecological impacts. The yellow-legged hornet, Vespa velutina was originally distributed throughout most of the Oriental region, but it has invasive populations in South Korea, Europe, and most recently, Japan. This species is a predator of honeybees, raising concerns about costs to beekeeping. A previous study concluded that South Korean and European populations originated from China. In this study, we investigate the genetic structure of V. velutina to infer the origin of Japanese populations. A maximum likelihood tree based on three mitochondrial genes (COI, Cytb, and 16S rRNA) revealed that V. velutina consists of an Indonesian–Malaysian clade and an Asian Continent clade, although some Indonesian samples are included in the latter clade. Sequences from individuals in the Japanese and South Korean populations were identical, suggesting that V. velutina in Japan came from South Korea. The single haplotype found in these introduced populations suggests that they originated from a very small number of founders from the natural distributional area. Nevertheless, their distribution continues to expand in introduced areas. Special attention should be paid to diapausing queens of the hornet, as they are likely responsible for these introductions.

Keywords

Genetic diversity Invasion Mitochondrial DNA Phylogeny Wasp 

References

  1. Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, Muller F, Fossoud A, Capdevielle-Dulac C, Torres-Leguizamon M, Chen XX, Tan JL, Jung C, Villemant C, Arnold G, Silvain JF (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biol Invasions 17:2357–2371CrossRefGoogle Scholar
  2. Arca M, Papachristoforou A, Mougel F, Rortais A, Monceau K, Bonnard O, Tardy P, Thiéry D, Silvain JF, Arnold G (2014) Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predtaor. Behav Process 106:122–129CrossRefGoogle Scholar
  3. Archer ME (1991) The number of species that can be recognised within the genus Vespa (Hym., Vespinae). Entomol Mon Mag 127:161–164Google Scholar
  4. Archer ME (2012) Vespine wasps of the world: behavior, ecology & taxonomy of the Vespinae. Siri Scientific Press, ManchesterGoogle Scholar
  5. Beggs JR, Brockerhoff EG, Corley JC, Kenis M, Masciocchi M, Muller F, Rome Q, Villemant C (2011) Ecological effects and management of invasive alien Vespidae. Biocontrol 56:505–526CrossRefGoogle Scholar
  6. Burne AR, Ritchie PA, Gruber MAM, Lester PJ (2016) A genetic bottleneck in populations of a New Zealand endemic ant associated with density of an invasive predatory wasp. Insectes Soc. doi:10.1007/s00040-016-0512-0 Google Scholar
  7. Choi MB, Martin SJ, Lee JW (2012) Distribution, spread, and impact of the invasive hornet Vespa velutina in South Korea. J Asia Pac Entomol 15:473–477CrossRefGoogle Scholar
  8. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi:10.1046/j.1365-294x.2000.01020.x CrossRefPubMedGoogle Scholar
  9. Drag L, Hauck D, Bérces S, Michalcewicz J, Jelaska ŠL, Aurenhammer S, Cizek L (2015) Genetic differentiation of populations of the threatened saproxylic beetle Rosalia longicorn, Rosalia alpina (Coleoptera: Cerambycidae) in Central and South-east Europe. Biol J Linn Soc 116:911–925CrossRefGoogle Scholar
  10. Handley LJL, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, Aebi A, Roy HE (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428CrossRefGoogle Scholar
  11. Jermiin LS, Crozier RH (1994) The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in Hymenoptera may be associated with nucleotide content. J Mol Evol 38:282–294CrossRefPubMedGoogle Scholar
  12. Jobb G (2011) TREEFINDER version of March 2011, Munich. http://www.treefinder.de
  13. Kanbe Y, Okada I, Yoneda M, Goka K, Tsuchida K (2008) Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften 95:1003–1008CrossRefPubMedGoogle Scholar
  14. Kim JK, Choi MB, Moon TY (2006) Occurrence of Vespa velutina Lepeletier from Korea, and a revised key for Korean Vespa species (Hymenoptera: Vespidae). Entomol Res 36:112–115CrossRefGoogle Scholar
  15. Kondo NI, Yamanaka D, Kanbe Y, Kunitake YK, Yoneda M, Tsuchida K, Goka K (2009) Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris. Naturwissenschaften 96:467–475CrossRefPubMedGoogle Scholar
  16. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404 CrossRefPubMedGoogle Scholar
  17. Lester PJ, Gruber MAM, Brenton-Rule EC, Archer M, Corley JC, Dvořák L, Masciocchi M, Van Oystaeyen A (2014) Determining the origin of invasions and demonstrating a lack of enemy release from microsporidian pathogens in common wasps (Vespula vulgaris). Divers Distrib 29:964–974CrossRefGoogle Scholar
  18. Minoshima YN, Yamane S, Ueno T (2015) An invasive alien hornet, Vespa velutina nigrithorax du Buysson (Hymenoptera, Vespidae), found in Kitakyushu, Kyushu Island: a first record of the species from mainland Japan. Jpn J Syst Entomol 21(2):259–261Google Scholar
  19. Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142CrossRefGoogle Scholar
  20. Moller H, Tilley JAV, Plunkett GM, Clapperton BK (1991) Nest sites of common and German wasps (Hymenoptera: Vespidae). N Z J Zool 18:121–125CrossRefGoogle Scholar
  21. Monceau K, Bonnard O, Thiéry D (2014) Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 87:1–16CrossRefGoogle Scholar
  22. Nguyen LTP, Saito F, Kojima J, Carpenter JM (2006) Vespidae of Viet Nam (Insecta: Hymenoptera) 2. taxonomic notes on Vespinae. Zool Sci 23:95–104CrossRefPubMedGoogle Scholar
  23. Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  24. Parnell J (2013) The biogeography of the Isthmus of Kura region: a review. Nord J Bot 31:1–15CrossRefGoogle Scholar
  25. Perrard A, Arca M, Rome Q, Muller F, Tan J, Bista S, Nugroho H, Baudoin R, Baylac M, Silvain JF, Carpenter JM, Villemant C (2014) Geographic variation of melanisation patterns in a hornet species: genetic differences, climatic pressures or aposematic constraints? PLoS One 9:e94162CrossRefPubMedPubMedCentralGoogle Scholar
  26. Perrard A, Pickett KM, Villemant C, Kojima J, Carpenter J (2013) Phylogeny of hornets: a total evidence approach (Hymenoptera, Vespidae, Vespinae, Vespa). J Hymenopt Res 32:1–15CrossRefGoogle Scholar
  27. Sakai Y, Takahashi J (2014) Discovery of a worker of Vespa velutina (Hymenoptera: Vespidae) from Tsushima Island, Japan. Jpn J Entomol New Ser 17(1):32–36 (Japanese with English summary) Google Scholar
  28. Shah FA, Shah TA (1991) Vespa velutina, a serious pest of honey bees in Kashmir. Bee World 72:161–164CrossRefGoogle Scholar
  29. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66CrossRefPubMedGoogle Scholar
  30. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701CrossRefGoogle Scholar
  31. Stahlhut JK, Fernández-Triana J, Adamowicz SJ, Buck M, Goulet H, Hebert PDN, Huber JT, Merilo MT, Sheffield CS, Woodcock T, Smith MA (2013) DNA barcoding reveals diversity of Hymenoptera and the dominance of parasitoids in a sub-arctic environment. BMC Ecol 13:2CrossRefPubMedPubMedCentralGoogle Scholar
  32. Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360CrossRefPubMedGoogle Scholar
  33. Takeuchi T, Takahashi J, Kiyoshi T, Nomura T, Tsubaki Y (2015) Genetic differentiation in the endangered myrmecophilous butterfly Niphanda fusca: a comparison of natural and secondary habitats. Conserv Genet 16:979–986CrossRefGoogle Scholar
  34. Tan K, Radloff SE, Li JJ, Hepburn HR, Yang MX, Zhang LJ, Neumann P (2007) Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94:469–472CrossRefPubMedGoogle Scholar
  35. Tsuchida K, Kudô K, Ishiguro N (2014) Genetic structure of an introduced paper wasp, Polistes chinensis antennalis (Hymenoptera: Vespidae) in New Zealand. Mol Ecol 23:4018–4034CrossRefPubMedGoogle Scholar
  36. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of invasive species. Proc Nat Acad Sci USA 97:5948–5953CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ueno T (2014) Establishment of the invasive hornet Vespa velutina (Hymenoptera: Vespidae) in Japan. Int J Chem Environ Biol Sci 2:220–222Google Scholar
  38. Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, Rome Q (2011) Predicting the invasion risk by the alien bee-hawking yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol Conserv 144:2142–2150CrossRefGoogle Scholar
  39. Wei SJ, Niu FF, Tan JL (2014) The mitochondrial genome of the Vespa bicolor Fabricius (Hymenoptera: Vespidae: Vespinae). Mitochondr DNA 27:875–876CrossRefGoogle Scholar
  40. Wilson EE, Holway DA (2010) Multiple mechanisms underlie displacement of solitary Hawaiian Hymenoptera by an invasive social wasp. Ecology 91:3294–3302CrossRefPubMedGoogle Scholar
  41. Wilson EE, Mullen LM, Holway DA (2009) Life history plasticity magnifies the ecological effects of a social wasp invasion. PNAS 106:12809–12813CrossRefPubMedPubMedCentralGoogle Scholar
  42. Woodruff DS (2003) The location of the Indochinese-Sundaic biogeographic transition in plants and birds. Nat Hist Bull Siam Soc 51:97–108Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2017

Authors and Affiliations

  • T. Takeuchi
    • 1
  • R. Takahashi
    • 1
  • T. Kiyoshi
    • 2
  • M. Nakamura
    • 3
  • Y. N. Minoshima
    • 4
  • J. Takahashi
    • 1
  1. 1.Faculty of Life SciencesKyoto Sangyo UniversityKyotoJapan
  2. 2.Department of ZoologyNational Museum of Nature and ScienceTsukubaJapan
  3. 3.Institute of Tropical Biology and ConservationUniversiti Malaysia SabahKota KinabaluMalaysia
  4. 4.Kitakyushu Museum of Natural History and Human HistoryKitakyushuJapan

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