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Population genetics of the invasive wasp Vespula germanica in South Africa

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Abstract

The German wasp (Vespula germanica) is a highly successful invader on a global scale. These wasps were first observed in the Western Cape region in South Africa in 1972, and they have the potential to expand their range and cause significant damage to the native biodiversity. Our study used nuclear (DNA microsatellites) and mitochondrial DNA (mtDNA) from 42 wasp colonies to analyse the population genetics of V. germanica in their invaded South African range. We sequenced three mitochondrial genes; cytochrome c oxidase I, cytochrome b and cytochrome c oxidase II. We found six mtDNA haplotypes present in South Africa. Although only a single fertilized queen is sufficient for the establishment of a wasp nest, the probability of a single introduced queen to successfully establish a nest and a population is very small. If multiple queens were introduced at the same time, the probability for more than one haplotype being transferred to the new population increases. Therefore, the true number of queen introductions occurred in South Africa can be inferred to be between two and six. We examined nine microsatellite loci and found weak-to-no genetic sub-structuring, likely due to high dispersal rates. We concluded that German wasps in South Africa maintain a homogenous population with movement of individuals between localities.

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References

  • Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518

    Article  Google Scholar 

  • Arca M, Capdevielle-Dulac C, Villemant C et al (2012) Development of microsatellite markers for the yellow-legged Asian hornet, Vespa velutina, a major threat for European bees. Conserv Genet Resour 4:283. https://doi.org/10.1007/s12686-011-9525-1

    Article  Google Scholar 

  • Archer ME (1998) The world distribution of the Euro-Asian species of Paravespula (Hym., Vespinae). Entomol Mon Mag 134:279–284

    Google Scholar 

  • Azzurro E, Golani D, Bucciarelli G, Bernardi G (2006) Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. J Exp Mar Biol Ecol 333:190–201

    Article  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Beggs JR, Brockerhoff EG, Corley JC et al (2011) Ecological effects and management of invasive alien Vespidae. Biocontrol 56:505–526

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, et al (1998) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France

  • Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429

    Article  PubMed  CAS  Google Scholar 

  • Bonckaert W, Vuerinckx K, Billen J, Hammond RL, Keller L, Wenseleers T (2008) Worker policing in the German wasp Vespula germanica. Behav Ecol 19:272–278

    Article  Google Scholar 

  • Brenton-Rule EC, Dobelmann J, Baty JW et al (2018) The origins of global invasions of the German wasp (Vespula germanica) and its infection with four honey bee viruses. Biol Invasions 20:3445–3460

    Article  Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  • Crozier RH, Page RE (1985) On being the right size: male contributions and multiple mating in social Hymenoptera. Behav Ecol Sociobiol 18:105–115

    Article  Google Scholar 

  • D’adamo P, Sackmann P, Corley JC, Rabinovich M (2002) The potential distribution of German wasps (Vespula germanica) in Argentina. N Z J Zool 29:79–85

    Article  Google Scholar 

  • Daly D, Archer ME, Watts PC et al (2002) Polymorphic microsatellite loci for eusocial wasps (Hymenoptera: Vespidae). Mol Ecol Notes 2:273–275

    CAS  Google Scholar 

  • de Villiers M, Kriticos DJ, Veldtman R (2017) Including irrigation in niche modelling of the invasive wasp Vespula germanica (Fabricius) improves model fit to predict potential for further spread. PLoS ONE 12:e0181397. https://doi.org/10.1371/journal.pone.0181397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dearden PK, Gemmell NJ, Mercier OR et al (2018) The potential for the use of gene drives for pest control in New Zealand: a perspective. J R Soc N Z 48:225–244

    Article  Google Scholar 

  • Ding G, Xu H, Oldroyd BP, Gloag RS (2017) Extreme polyandry aids the establishment of invasive populations of a social insect. Heredity 119:381–387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  PubMed  CAS  Google Scholar 

  • Dobelmann J, Loope KJ, Wilson-Rankin E et al (2017) Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126:1208–1218

    Article  CAS  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130

    Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Foster KR, Ratnieks FLW, Gyllenstrand N, Thorén PA (2001) Colony kin structure and male production in Dolichovespula wasps. Mol Ecol 10:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Giliomee JH (2011) Recent establishment of many alien insects in South Africa: a cause for concern. Afr Entomol 19:151–155

    Article  Google Scholar 

  • Gloag R, Ding G, Christie JR et al (2017) An invasive social insect overcomes genetic load at the sex locus. Nat Ecol Evol 1:0011. https://doi.org/10.1038/s41559-016-0011

    Article  Google Scholar 

  • Goodisman MAD, Matthews RW, Crozier RH (2001) Hierarchical genetic structure of the introduced wasp Vespula germanica in Australia. Mol Ecol 10:1423–1432

    Article  PubMed  CAS  Google Scholar 

  • Goodisman MA, Matthews RW, Crozier RH (2002) Mating and reproduction in the wasp Vespula germanica. Behav Ecol Sociobiol 51:497–502

    Article  Google Scholar 

  • Hasegawa E, Takahashi J (2002) Microsatellite loci for genetic research in the hornet Vespa mandarinia and related species. Mol Ecol Notes 2:306–308

    Article  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  PubMed  CAS  Google Scholar 

  • Haupt K (2015) Assessment of the invasive wasp Vespula germanica in South Africa. M.Sc. Thesis. University of Stellenbosch

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Johansson H, Seppa P et al (2018) Weak population structure in the ant Formica fusca. PeerJ 6:e5024. https://doi.org/10.7717/peerj.5024

    Article  PubMed  PubMed Central  Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evol (N Y) 48:694–704

    Google Scholar 

  • Kenis M, Auger-Rozenberg M-A, Roques A et al (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lester PJ, Beggs JR (2019) Invasion success and management strategies for social Vespula wasps. Annu Rev Entomol 64:51–71

    Article  PubMed  CAS  Google Scholar 

  • Lester PJ, Gruber MAM, Brenton-Rule EC et al (2014) Determining the origin of invasions and demonstrating a lack of enemy release from microsporidian pathogens in common wasps (Vespula vulgaris). Divers Distrib 20:964–974

    Article  Google Scholar 

  • Loope KJ, Chien C, Juhl M (2014) Colony size is linked to paternity frequency and paternity skew in yellowjacket wasps and hornets. BMC Evol Biol 14:277. https://doi.org/10.1186/s12862-014-0277-x

    Article  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2004) 100 of the World’s Worst Invasive Alien Species: a selection from the Global Invasive Species Database. Invasive Species. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)

  • Markert JA, Champlin DM, Gutjahr-Gobell R et al (2010) Population genetic diversity and fitness in multiple environments. BMC Evol Biol 10:205. https://doi.org/10.1186/1471-2148-10-205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marsden CD, Ortega-Del Vecchyo D, O’Brien DP et al (2016) Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc Natl Acad Sci USA 113:152–157

    Article  PubMed  CAS  Google Scholar 

  • Masciocchi M, Corley J (2013) Distribution, dispersal and spread of the invasive social wasp (Vespula germanica) in Argentina. Austral Ecol 38:162–168

    Article  Google Scholar 

  • Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Nieminen M, Singer MC, Fortelius W et al (2001) Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am Nat 157:237–244

    Article  PubMed  CAS  Google Scholar 

  • Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos PM, Stevens HH, Wagner H (2019) vegan: Community Ecology Package. R package version 2.3–5.   http://CRAN.R-project.org/package=vegan

  • Passera L (1994) Characteristics of tramp species. In: Williams DF (ed) Exotic ants: biology, impact and control of introduced species. Westview Press, Oxford, pp 23–43

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55

    Article  Google Scholar 

  • Richardson DM, Macdonald IAW, Forsyth GG (1989) Reductions in plant species richness under stands of alien trees and shrubs in the Fynbos biome. South Afr For J 149:1–8

    Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sackmann P, Rabinovich M, Corley JC (2001) Successful removal of German yellowjackets (Hymenoptera: Vespidae) by toxic baiting. J Econ Entomol 94:811–816

    Article  PubMed  CAS  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schmack JM, Brenton-Rule EC, Veldtman R et al (2019) Lack of genetic structuring, low effective population sizes and major bottlenecks characterise common and German wasps in New Zealand. Biol Invasions 21:3185–3201

    Article  Google Scholar 

  • Spradbery JP, Maywald GF (1992) The distribution of the European or German wasp, Vespula germanica (F.) (Hymenoptera: Vespidae), in Australia: past, present and future. Aust J Zool 40:495–510

    Article  Google Scholar 

  • Sutton JT, Robertson BC, Jamieson IG (2011) Dye shift: a neglected source of genotyping error in molecular ecology. Mol Ecol Resour 11:514–520

    Article  PubMed  CAS  Google Scholar 

  • Thomas CR (1960) The European wasp (Vespula germanica Fab.) in New Zealand. DSIR Information Series No. 27

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thorén PA, Paxton RJ, Estoup A (1995) Unusually high frequency of (CT)n and (GT)n microsatellite loci in a yellowjacket wasp, Vespula rufa (L.) (Hymenoptera: Vespidae). Insect Mol Biol 4:141–148

    Article  PubMed  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • van Wilgen BW, De Lange WJ (2011) The costs and benefits of biological control of invasive alien plants in South Africa. Afr Entomol 19:504–514

    Article  Google Scholar 

  • Vandewoestijne S, Schtickzelle N, Baguette M (2008) Positive correlation between genetic diversity and fitness in a large, well-connected metapopulation. BMC Biol 6:46. https://doi.org/10.1186/1741-7007-6-46

    Article  PubMed  PubMed Central  Google Scholar 

  • Veldtman R, Addison P, Tribe GD (2012) Current status and potential future impact of invasive vespid wasps (Vespula germanica and Polistes dominulus) in South Africa. IOBC/WPRS Bull 75:217–227

    Google Scholar 

  • Whitehead VB, Prins AJ (1975) The European wasp, Vespula germanica (F.), in the Cape Peninsula. J Entomol Soc South Afr 38:39–42

    Google Scholar 

  • Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. Proc Natl Acad Sci USA 102:13367–13371

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by Victoria University of Wellington. We thank Julia Schmack for sharing her DNA microsatellite data with us and two anonymous reviewers for their useful comments that improved our original manuscript.

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Correspondence to J. Eloff.

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Eloff, J., Veldtman, R., Bulgarella, M. et al. Population genetics of the invasive wasp Vespula germanica in South Africa. Insect. Soc. 67, 229–238 (2020). https://doi.org/10.1007/s00040-020-00752-x

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