Abstract
Invasive species cause severe ecological and economic impacts in their introduced ranges. Vespula wasps, native to Eurasia, are a major threat to New Zealand native ecosystems. Understanding factors that influence the success of wasp invasion is pivotal for the development of control strategies. Here, we compare genetic diversity and structure of Vespula germanica and Vespula vulgaris between regions of their native and introduced ranges using microsatellite markers. Our study found lower diversity and lack of genetic structure for both invasive Vespula species within New Zealand. The significant reduction in allelic richness, gene diversity and effective population size illustrate a major bottleneck in New Zealand V. germanica and V. vulgaris populations. Strong signatures of population structure were found for both Vespula species with two clusters being identified as optimal k, approximately corresponding to the native and the invaded ranges. Our results highlight the fact that the lack of genetic diversity does not impede successful invasions in V. germanica and V. vulgaris and encourage further research into mechanisms that promote the success of invasive social insects. Overall, this study provides insights into the genetics of invasive Vespula wasps that can be useful for the development of efficient management strategies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akre RD, Reed HC (1981) Population cycles of yellowjackets (Hymenoptera: Vespinae) in the Pacific Northwest. Environ Entomol 10(3):267–274
Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30
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
Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, Muller F et al (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biol Invasions 17:2357–2371. https://doi.org/10.1007/s10530-015-0880-9
Beggs JR, Rees JS (1999) Restructuring of Lepidoptera communities by introduced Vespula wasps in a New Zealand beech forest. Oecologia 119:565–571
Beggs JR, Toft RJ, Malham JP et al (1998) The difficulty of reducing introduced wasp (Vespula vulgaris) populations for conservation gains. N Z J Ecol 22:55–63
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. https://doi.org/10.1007/s10526-011-9389-z
Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1998) GENETIX, Logiciel sous Windows pour la Génétique des Populations. Laboratoire Génome et Populations. CNRS UPR 9060. Université de Montpellier II, Montpellier
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. https://doi.org/10.1016/S0092-8674(03)00606-8
Brenton-Rule EC, Dobelmann J, Baty JW, Brown RL, Dvorak L 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
Burne AR, Ritchie PA, Gruber M, Lester PJ (2017) A genetic bottleneck in populations of a New Zealand endemic ant associated with density of an invasive predatory wasp. Insectes Soc 64:65–74
Carlsson J (2008) Effects of microsatellite null allele on assignment testing. J Hered 99:616–623
Chapman RE, Bourke AF (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662
Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195
Chau LM, Hanna C, Jenkins LT, Kutner RE, Burns EA, Kremen C, Goodisman MAD (2015) Population genetic structure of the predatory, social wasp Vespula pensylvanica in its native and invasive range. Ecol Evol 5:5573–5587. https://doi.org/10.1002/ece3.1757
Cheng D, Liang G, Xu Y (2016) Meta-analysis reveals asymmetric reduction in the genetic diversity of introduced populations of exotic insects. Biol Invasions 18:1163–1175. https://doi.org/10.1007/s10530-016-1058-9
Clapperton BK, Moller H, Sandlant GR (1989) Distribution of social wasps (Hymenoptera: Vespidae) in New Zealand in 1987. N Z J Zool 16:315–323. https://doi.org/10.1080/03014223.1989.10422896
Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110
Corin S, Abbott K, Ritchie P, Lester PJ (2007) Large scale unicoloniality: the population and colony structure of the invasive Argentine ant (Linepithema humile) in New Zealand. Insect Soc 54:275–282. https://doi.org/10.1007/s00040-007-0942-9
Daly D, Archer ME, Watts PC et al (2002) Polymorphic microsatellite loci for eusocial wasps (Hymenoptera: Vespidae). Mol Ecol Notes 2:273–275
Davis LM, Glenn TC, Elsey RM, Dessauer HC, Sawyer RH (2001) Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis. Mol Ecol 10:1011–1024. https://doi.org/10.1046/j.1365-294X.2001.01241.x
Department of Conservation and Ministry of the Environment (2000) The New Zealand biodiversity strategy 2000–2020. Department of Conservation and Ministry of the Environment. ISBN: O-478-21919-9
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
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214
Dobelmann J, Loope KJ, Wilson-Rankin E, Quinn O, Baty JW, Gruber MAM, Lester PJ (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. https://doi.org/10.1111/oik.04117
Donovan BJ (1984) Occurrence of the common wasp, Vespula vulgaris (L.) (Hymenoptera: Vespidae) in New Zealand. N Z J Zool 11:417–427. https://doi.org/10.1080/03014223.1984.10428256
Donovan BJ, Howie A, Schroeder NC, Wallace AR, Read P (1992) Comparative characteristics of nests of Vespula germanica (F.) and Vespula vulgaris (L.) (Hymenoptera: Vespinae) from Christchurch City, New Zealand. N Z J Zool 19:61–71
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
Edgar GJ, Stuart-Smith RD, Thomson RJ, Freeman DJ (2017) Consistent multi-level trophic effects of marine reserve protection across northern New Zealand. PLoS ONE 12:e0177216. https://doi.org/10.1371/journal.pone.0177216
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
Excoffier L, Lischer HEL (2010) Arlequin Suite Ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Foster KR, Ratnieks FLW, Gyllenstrand N, Thorén PA (2001) Colony kin structure and male production in Dolichovespula wasps. Mol Ecol 10:1003–1010
Gardner-Gee R, Beggs JR (2013) Invasive wasps, not birds, dominate in a temperate honeydew system. Austral Ecol 38:346–354
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079. https://doi.org/10.1073/pnas.092694199
Gloag R, Ding G, Christie JR, Buchmann G, Beekman M, Oldroyd BP (2017) An invasive social insect overcomes genetic load at the sex locus. Nat Ecol Evol 1:0011
Golani D, Azzurro E, Corsini-Foka M, Falautano M, Andaloro F, Bernardi G (2007) Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biol Lett 3:541–545. https://doi.org/10.1098/rsbl.2007.0308
Goodisman MA, Matthews RW, Crozier RH (2001) Hierarchical genetic structure of the introduced wasp Vespula germanica in Australia. Mol Ecol 10:1423–1432
Goodisman M, Sankovich K, Kovacs J (2007) Genetic and morphological variation over space and time in the invasive fire ant Solenopsis invicta. Biol Invasions 9:571–584. https://doi.org/10.1007/s10530-006-9059-8
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-Statistics. J Hered 86:485–486
Hanna C, Cook E, Thompson A, Dare L, Palaski A, Foote D, Goodisman M (2014) Colony social structure in native and invasive populations of the social wasp Vespula pensylvanica. Biol Invasions 16:283–294. https://doi.org/10.1007/s10530-013-0517-9
Hasegawa E, Takahashi J (2002) Microsatellite loci for genetic research in the hornet Vespa mandarinia and related species. Mol Ecol Notes 2:306–308
Hoffman EA, Kovacs JL, Goodisman MAD (2008) Genetic structure and breeding system in a social wasp and its social parasite. BMC Evol Biol 8:239. https://doi.org/10.1186/1471-2148-8-239
Holm S (1979) A simple sequential rejective method procedure. Scand J Stat 6:65–70
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18. https://doi.org/10.1111/j.1365-2664.2008.01600.x
Husseneder C, Simms D, Delatte J, Wang C, Grace J, Vargo E (2012) Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus. Biol Invasions 14:419–437. https://doi.org/10.1007/s10530-011-0087-7
Johnson RN, Starks PT (2004) A surprising level of genetic diversity in an invasive wasp: Polistes dominulus in the northeastern United States. Ann Entomol Soc Am 97:732–737
Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977. https://doi.org/10.1111/j.1365-294X.2008.03902.x
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Kenis M, Auger-Rozenberg M, Roques A, Timms L, Péré C, Cock M, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45. https://doi.org/10.1007/s10530-008-9318-y
Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177
Laugier G, Le Moguédec G, Su W, Tayeh A, Soldati L, Serrate B, Estoup A, Facon B (2016) Reduced population size can induce quick evolution of inbreeding depression in the invasive ladybird Harmonia axyridis. Biol Invasions 18:2871–2881. https://doi.org/10.1007/s10530-016-1179-1
Leathwick DM, Godfrey PL (1996) Overwintering colonies of the common wasp (Vespula vulgaris) in Palmerston North, New Zealand. N Z J Zool 23:355–358
Lester PJ, Beggs JR (2019) Invasion success and management strategies for social Vespula wasps. Annu Rev Entomol 64:51–71. https://doi.org/10.1146/annurev-ento-011118-111812
Lester PJ, Beggs JR, Brown RL, Edwards ED, Groenteman R, Toft RJ, Twidle AM, Ward DF (2013) The outlook for control of New Zealand’s most abundant, widespread and damaging invertebrate pests: social wasps. N Z Sci Rev 70:56–62
Lester PJ, Gruber MAM, Brenton-Rule E, Archer M, Corley JC, Dvořák L, Masciocchi M, Oystaeyen A (2014) Determining the origin of invasions and demonstrating a lack of enemy release from microsporidian pathogens in the common wasps (Vespula vulgaris). Divers Distrib 20:964–974
Loope KJ, Millar JG, Wilson Rankin EE (2018) Weak nestmate discrimination behavior in native and invasive populations of a yellowjacket wasp (Vespula pensylvanica). Biol Invasions 20:3431–3444
Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373. https://doi.org/10.1007/s10592-010-0050-7
Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142
Moller H, Clapperton BK, Alspach PA, Tilley J (1991) Comparative seasonality of Vespula germanica (F.) and Vespula vulgaris (L.) colonies (Hymenoptera: Vespidae) in urban Nelson, New Zealand. N Z J Zool 18:111–120
Moore J, Nelson N, Keall S, Daugherty C (2008) Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara). Conserv Genet 9:1243–1251. https://doi.org/10.1007/s10592-007-9452-6
Murray J (1964) Multiple mating and effective population size in Cepaea nemoralis. Evolution 18:283. https://doi.org/10.2307/2406402
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Parkes J, Byrom A, Edge K (2017) Eradicating mammals on New Zealand island reserves: what is left to do? N Z J Ecol 41:263–270. https://doi.org/10.20417/nzjecol.41.25
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
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
Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. J Hered 92:206
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
Plunkett GM, Moller H, Hamilton C, Clapperton BK, Thomas CD (1989) Overwintering colonies of German (Vespula germanica) and common wasps (Vespula vulgaris) (Hymenoptera: Vespidae) in New Zealand. N Z J Zool 16:345–353
Pritchard JC, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Puillandre N, Dupas S, Dangles O, Zeddam J, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333
Purcell KM, Ling N, Stockwell CA (2012) Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biol Invasions 14:2057–2065
Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237. https://doi.org/10.1046/j.1523-1739.2003.01236.x
Rico C, Cuesta JA, Drake P, Macpherson E, Bernatchez L, Marie AD (2017) Null alleles are ubiquitous at microsatellite loci in the Wedge Clam (Donax trunculus). PeerJ 5:e3188. https://doi.org/10.7717/peerj.3188
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Russell JC, Meyer J, Holmese ND, Pagad S (2017) Invasive alien species on islands: impacts, distribution, interactions and management. Environ Conserv 44:359–370. https://doi.org/10.1017/S0376892917000297
Sala E, Giakoumi S (2018) No-take marine reserves are the most effective protected areas in the ocean. ICES J Mar Sci 75:1166–1168. https://doi.org/10.1093/icesjms/fsx059
Schmid-Hempel P, Schmid-Hempel R, Brunner PC, Seeman OD, Allen GR (2007) Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99:414–422. https://doi.org/10.1038/sj.hdy.6801017
Secretariat of the Convention on Biological Diversity (2004) The ecosystem approach. Secretariat of the Convention on Biological Diversity. ISBN: 92-9225-023-x
Sherpa S, Rioux D, Pougnet-Lagarde C, Després L (2018) Genetic diversity and distribution differ between long-established and recently introduced populations in the invasive mosquito Aedes albopictus. Infect Genet Evol 58:145–156
Shurtliff QR, Pearse DE, Rogers DS (2005) Parentage analysis of the canyon mouse (Peromyscus crinitus): evidence for multiple paternity. J Mammal 86:531–540. https://doi.org/10.1644/1545-1542(2005)86[531:PAOTCM]2.0.CO;2
Sonsthagen SA, Wilson RE, Underwood JG (2017) Genetic implications of bottleneck effects of differing severities on genetic diversity in naturally recovering populations: an example from Hawaiian coot and Hawaiian gallinule. Ecol Evol 7:9925–9934. https://doi.org/10.1002/ece3.3530
Spradbery JP (1973) Wasps: an account of the biology and natural history of solitary and social wasps. University of Washington Press, Seattle
Suarez AV, Holway DA, Liang D, Tsutsui ND, Case TJ (2002) Spatiotemporal patterns of intraspecific aggression in the invasive Argentine ant. Anim Behav 64:697–708
Suarez AV, Robinson GE, Toth AL, Smith CR (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9:735–748. https://doi.org/10.1038/nrg2429
Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155
Sutton JT, Robertson BC, Jamieson IG (2011) Dye shift: a neglected source of genotyping error in molecular ecology. Mol Ecol Resour 11:514–520. https://doi.org/10.1111/j.1755-0998.2011.02981.x
Takeuchi T, Takahashi R, Kiyoshi T, Nakamura M, Minoshima Y, Takahashi J (2017) The origin and genetic diversity of the yellow-legged hornet, Vespa velutina introduced in Japan. Insect Soc 64:313–320. https://doi.org/10.1007/s00040-017-0545-z
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
Toft RJ, Rees JS (1998) Reducing predation of orb-web spiders by controlling common wasps (Vespula vulgaris) in a New Zealand beech forest. Ecol Entomol 23:90–95. https://doi.org/10.1046/j.1365-2311.1998.00100.x
Tsuchida K, Kudô K, Ishiguro N (2014) Genetic structure of an introduced paper wasp, Polistes chinensis antennalis (Hymenoptera, Vespidae) in New Zealand. Mol Ecol 23:4018–4034. https://doi.org/10.1111/mec.12852
Tsutsui ND, Case TJ (2001) Population genetics and colony structure of the Argentine ant (Linepithema humile) in its native and introduced ranges. Evolution 55:976–985. https://doi.org/10.1111/j.0014-3820.2001.tb00614.x
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
van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403. https://doi.org/10.1146/annurev.ento.54.110807.090443
Visscher PK, Vetter RS (2003) Annual and multi-year nests of the western yellowjacket, Vespula pensylvanica, in California. Insect Soc 50:160–166. https://doi.org/10.1007/s00040-003-0636-x
Wang J, Santiago E, Caballero A (2016) Prediction and estimation of effective population size. Heredity 117:193
Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189:633–644
Whiting PW (1933) Selective fertilization and sex-determination in Hymenoptera. Science 78:537–538
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97
Zayed A (2004) Effective population size in Hymenoptera with complementary sex determination. Heredity 93:627
Zayed A, Packer L (2007) The population genetics of a solitary oligolectic sweat bee, Lasioglossum (Sphecodogastra) oenotherae (Hymenoptera: Halictidae). Heredity 99:397
Zayed A, Constantin ŞA, Packer L (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2:e868
Zhang M, Evans TA (2017) Determining urban exploiter status of a termite using genetic analysis. Urban Ecosyst 20:535–545
Acknowledgements
Thanks to the landowners and managers for access to the various sites for collecting wasps. We thank Jana Dobelmann who shared V. vulgaris DNA extractions, Carolien van Zyl for sharing South African V. germanica samples from her PhD project and Dr Lara Shepherd who helped with analyses. We also thank two anonymous referees and the Handling Editor for their useful comments that improved our manuscript.
Funding
This work was partially funded by the Ministry of Business, Innovation and Employment (New Zealand’s Biological Heritage NSC, C09X1501) and by Victoria University of Wellington.
Author information
Authors and Affiliations
Contributions
JMS collected the New Zealand samples and together with JPL and JRB conceived the project. ECBR, RV and TW collected or provided samples. MB and JMS led the genetic work, analysed and interpreted the data. JMS and MB led the writing with input from all authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schmack, J.M., Brenton-Rule, E.C., Veldtman, R. et al. Lack of genetic structuring, low effective population sizes and major bottlenecks characterise common and German wasps in New Zealand. Biol Invasions 21, 3185–3201 (2019). https://doi.org/10.1007/s10530-019-02039-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-019-02039-0