Biological Invasions

, Volume 18, Issue 4, pp 935–952 | Cite as

Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences

  • Jeff R. GarnasEmail author
  • Marie-Anne Auger-Rozenberg
  • Alain Roques
  • Cleo Bertelsmeier
  • Michael J. Wingfield
  • Davina L. Saccaggi
  • Helen E. Roy
  • Bernard Slippers
Insect Invasions


The advent of simple and affordable tools for molecular identification of novel insect invaders and assessment of population diversity has changed the face of invasion biology in recent years. The widespread application of these tools has brought with it an emerging understanding that patterns in biogeography, introduction history and subsequent movement and spread of many invasive alien insects are far more complex than previously thought. We reviewed the literature and found that for a number of invasive insects, there is strong and growing evidence that multiple introductions, complex global movement, and population admixture in the invaded range are commonplace. Additionally, historical paradigms related to species and strain identities and origins of common invaders are in many cases being challenged. This has major consequences for our understanding of basic biology and ecology of invasive insects and impacts quarantine, management and biocontrol programs. In addition, we found that founder effects rarely limit fitness in invasive insects and may benefit populations (by purging harmful alleles or increasing additive genetic variance). Also, while phenotypic plasticity appears important post-establishment, genetic diversity in invasive insects is often higher than expected and increases over time via multiple introductions. Further, connectivity among disjunct regions of global invasive ranges is generally far higher than expected and is often asymmetric, with some populations contributing disproportionately to global spread. We argue that the role of connectivity in driving the ecology and evolution of introduced species with multiple invasive ranges has been historically underestimated and that such species are often best understood in a global context.


Admixture Bridgehead effects Invasion genetics Invasive species management Multiple introductions 



The Tree Protection Cooperative Programme (TPCP), the National Research Foundation (NRF) and the Department of Trade and Industry (DTI) of South Africa are acknowledged for their financial support. This paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted by the DST-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, in November 2014. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop.

Supplementary material

10530_2016_1082_MOESM1_ESM.xlsx (107 kb)
Supplementary material 1 (XLSX 107 kb)


  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. doi: 10.1007/s10530-015-0880-9 Google Scholar
  2. Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Proc R Soc Lond [Biol] 360:1813–1823Google Scholar
  3. Auger-Rozenberg MA, Roques A (2012) Seed wasp invasions promoted by unregulated seed trade affect vegetal and animal biodiversity. Integr Zool 7:228–246PubMedCrossRefGoogle Scholar
  4. Aukema JE, Mccullough DG, Von Holle B, Liebhold A, Britton K, Frankel SJ (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897CrossRefGoogle Scholar
  5. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–168Google Scholar
  6. Balanyà J, Huey RB, Gilchrist GW, Serra L (2009) The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364–367PubMedCrossRefGoogle Scholar
  7. Barrett S (2015) Foundations of invasion genetics: the Baker and Stebbins legacy. Mol Ecol 24:1927–1941PubMedCrossRefGoogle Scholar
  8. Bergeron M-J, Leal I, Foord B, Ross G, Davis C, Slippers B, de Groot P, Hamelin RC (2011) Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada. Fungal Biol 115:750–758PubMedCrossRefGoogle Scholar
  9. Bohmann K, Evans A, Gilbert MTP, Carvalho GR, Creer S, Knapp M, Yu DW, de Bruyn M (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol 29:358–367PubMedCrossRefGoogle Scholar
  10. Boissin E, Hurley B, Wingfield MJ, Vasaitis R, Stenlid J, Davis C, De Groot P, Ahumada R, Carnegie A, Goldarazena A, Klasmer P, Wermelinger B, Slippers B (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744PubMedCrossRefGoogle Scholar
  11. Bolnick DI, Svanback R, Araujo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104:10075–10079PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11PubMedCrossRefGoogle Scholar
  13. Boubou A, Migeon A, Roderick GK, Auger P, Cornuet J-M, Magalhaes S, Navajas M (2012) Test of colonisation scenarios reveals complex invasion history of the Red Tomato Spider Mite Tetranychus evansi. PLoS ONE 7:e35601PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boyd IL, Freer-Smith PH, Gilligan CA, Godfray HC (2013) The consequence of tree pests and diseases for ecosystem services. Science 342:1235773PubMedCrossRefGoogle Scholar
  15. Bryant EH, Meffert LM (1993) The effect of serial founder-flush cycles on quantitative genetic variation in the housefly. Heredity 70:122–129CrossRefGoogle Scholar
  16. Carew M, Schiffer M, Umina P, Weeks A, Hoffmann A (2009) Molecular markers indicate that the wheat curl mite, Aceria tosichella Keifer, may represent a species complex in Australia. Bull Entomol Res 99:479–486PubMedCrossRefGoogle Scholar
  17. Caron V, Ede FJ, Sunnucks P (2014) Unravelling the paradox of loss of genetic variation during invasion: superclones may explain the success of a clonal invader. PLoS ONE 9:e97744PubMedPubMedCentralCrossRefGoogle Scholar
  18. Castrillo LA, Hajek AE, Pajares JA, Thomsen IM, Csóka G, Kenaley SC, Kepler RM, Zamora P, Angeli S (2015) Multilocus genotyping of Amylostereum spp. associated with Sirex noctilio and other woodwasps from Europe reveal clonal lineage introduced to the US. Fungal Biol. doi: 10.1016/j.funbio.2015.03.004 Google Scholar
  19. Chapple DG, Miller KA, Kraus F, Thompson MB (2013) Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Divers Distrib 19:134–146CrossRefGoogle Scholar
  20. Charlesworth J, Eyre-Walker A (2007) The other side of the nearly neutral theory, evidence of slightly advantageous back-mutations. Proc Natl Acad Sci USA 104:16992–16997PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chown SL, Hodgins KA, Griffin PC, Oakeshott JG, Byrne M, Hoffmann AA (2014) Biological invasions, climate change and genomics. Evol Appl 8:23–46PubMedPubMedCentralCrossRefGoogle Scholar
  22. Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627PubMedCrossRefGoogle Scholar
  23. Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dickson R (1962) Development of the spotted alfalfa aphid population in North America. Internationaler Kongress für Entomologie, Vienna 1960, pp 26–28Google Scholar
  25. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92PubMedCrossRefGoogle Scholar
  26. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  27. Dlugosch KM, Anderson SR, Braasch J, Cang FA, Gillette HD (2015) The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Mol Ecol 24:2095–2111PubMedCrossRefGoogle Scholar
  28. Dybdahl M, Kane S (2005) Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecol 86:1592–1601CrossRefGoogle Scholar
  29. Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  30. Eschen R, Britton K, Brockerhoff E, Burgess T, Dalley V, Epanchin-Niell RS, Gupta K, Hardy G, Huang Y, Kenis M, Kimani E, Li HM, Olsen S, Ormrod R, Otieno W, Sadof C, Tadeu E, Theyse M (2015) International variation in phytosanitary legislation and regulations governing importation of plants for planting. Environ Sci Pol 51:228–237CrossRefGoogle Scholar
  31. Essl F, Bacher S, Blackburn TM, Booy O, Brundu G, Brunel S, Cardoso A-C, Eschen R, Gallardo B, Galil B, García-Berthou E, Genovesi P, Groom Q, Harrower C, Hulme PE, Katsanevakis S, Kenis M, Kühn I, Kumschick S, Martinou AF, Nentwig W, O’Flynn C, Pagad S, Pergl J, Pyšek P, Rabitsch W, Richardson DM, Roques A, Roy HE, Scalera R, Schindler S, Seebens H, Vanderhoeven S, Vilà M, Wilson JRU, Zenetos A, Jeschke JM (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782CrossRefGoogle Scholar
  32. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130PubMedCrossRefGoogle Scholar
  33. Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E, Vitalis R, Guillemaud T, Lundgren JG, Estoup A (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427PubMedCrossRefGoogle Scholar
  34. Fisher MC, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194PubMedCrossRefGoogle Scholar
  35. Follett PA, Neven LG (2006) Current trends in quarantine entomology. Annu Rev Entomol 51:359–385PubMedCrossRefGoogle Scholar
  36. Garnas JR, Drummond FA, Groden E (2007) Intercolony aggression within and among local populations of the invasive ant, Myrmica rubra (Hymenoptera: Formicidae), in coastal Maine. Environ Entomol 36:105–113PubMedCrossRefGoogle Scholar
  37. Garnas JR, Hurley BP, Slippers B, Wingfield MJ (2012) Biological control of forest plantation pests in an interconnected world requires greater international focus. Int J Pest Manag 58:211–223CrossRefGoogle Scholar
  38. Gilabert A, Simon J-C, Dedryver C-A, Plantegenest M (2014) Do ecological niches differ between sexual and asexual lineages of an aphid species? Evol Ecol 28:1095–1104CrossRefGoogle Scholar
  39. Gladieux P, Feurtey A, Hood ME, Snirc A, Clavel J, Dutech C, Roy M, Giraud T (2015) The population biology of fungal invasions. Mol Ecol 24:1969–1986PubMedCrossRefGoogle Scholar
  40. Gleman S (2003) How are deleterious mutations purged? Drift versus random mating. Evolution 57:2678–2687CrossRefGoogle Scholar
  41. Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454CrossRefGoogle Scholar
  42. Haack RA, Britton KO, Brockerhoff EG, Cavey JF, Garrett LJ, Kimberley M, Lowenstein F, Nuding A, Olson LJ, Turner J, Vasilaky KN (2014) Effectiveness of the International Phytosanitary Standard ISPM No. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. PLoS ONE 9:e96611PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hajek AE, Nielsen C, Kepler RM, Long SJ, Castrillo L (2013) Fidelity among Sirex woodwasps and their fungal symbionts. Microb Ecol 65:753–762PubMedPubMedCentralCrossRefGoogle Scholar
  44. Haran J, Koutroumpa F, Magnoux E, Roques A, Roux G (2015) Ghost mtDNA haplotypes generated by fortuitous NUMTs can deeply disturb infra-specific genetic diversity and phylogeographic pattern. J Zool Syst Evol Res 53:109–115CrossRefGoogle Scholar
  45. Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750CrossRefGoogle Scholar
  46. Hellenthal G, Busby GB, Band G, Wilson JF, Capelli C, Falush D, Myers S (2014) A genetic atlas of human admixture history. Science 343:747–751PubMedPubMedCentralCrossRefGoogle Scholar
  47. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256PubMedCrossRefGoogle Scholar
  48. Hoffmann AA, Reynolds KT, Nash MA, Weeks AR (2008) A high incidence of parthenogenesis in agricultural pests. Proc R Soc Lond [Biol] 275:2473–2481CrossRefGoogle Scholar
  49. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309PubMedCrossRefGoogle Scholar
  50. Hughes AL (2012) Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity 108:347–353PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  52. Hulcr J, Dunn RR (2011) The sudden emergence of pathogenicity in insect-fungus symbioses threatens naive forest ecosystems. Proc R Soc Lond [Biol] 278:2866–2873CrossRefGoogle Scholar
  53. Hurley BP, Garnas J, Wingfield MJ, Branco M, Richardson DM, Slippers B (2016) Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biol Invasions. doi: 10.1007/s10530-016-1081-x
  54. Jarvis JP, Cropp SN, Vaughn TT, Pletscher LS, King-Ellison K, Adams-Hunt E, Erickson C, Cheverud JM (2011) The effect of a population bottleneck on the evolution of genetic variance/covariance structure. J Evol Biol 24:2139–2152PubMedCrossRefGoogle Scholar
  55. Jerde JL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157CrossRefGoogle Scholar
  56. Jones EI, Gomulkiewicz R (2012) Biotic interactions, rapid evolution, and the establishment of introduced species. Am Nat 179:E28–E36PubMedCrossRefGoogle Scholar
  57. Keller SR, Taylor DR (2010) Genomic admixture increases fitness during a biological invasion. J Evol Biol 23:1720–1731PubMedCrossRefGoogle Scholar
  58. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  59. Keller SR, Fields PD, Berardi AE, Taylor DR (2014) Recent admixture generates heterozygosity-fitness correlations during the range expansion of an invading species. J Evol Biol 27:616–627PubMedCrossRefGoogle Scholar
  60. Kerdelhué C, Boivin T, Burban C (2014) Contrasted invasion processes imprint the genetic structure of an invasive scale insect across southern Europe. Heredity 113:390–400PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kerdelhué C, Battisti A, Burban C, Branco M, Cassel-Lundhagen A, İpekdal K, Larsson S, Lopez-Vaamonde C, Magnoux E, Mateus E, Mendel Z, Negrisolo E, Paiva M-R, Pivotto ID, Rocha S, Ronnås C, Roques A, Rossi J-P, Rousselet J, Salvato P, Santos H, Simonato M, Zane L (2015) Genetic diversity and structure at different spatial scales in the processionary moths. In: Roques A (ed) Processionary moths and climate change: an update. Springer, Dordrecht, pp 163–226Google Scholar
  62. Kolbe JJ, Glor RE, Schettino L, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  63. Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591PubMedCrossRefGoogle Scholar
  64. Krehenwinkel H, Tautz D (2013) Northern range expansion of European populations of the wasp spider Argiope bruennichi is associated with global warming-correlated genetic admixture and population-specific temperature adaptations. Mol Ecol 22:2232–2248PubMedCrossRefGoogle Scholar
  65. Lanfear R, Kokko H, Eyre-Walker A (2014) Population size and the rate of evolution. Trends Ecol Evol 29:33–41PubMedCrossRefGoogle Scholar
  66. Lawson Handley LJ (2015) How will the ‘molecular revolution’ contribute to biological recording? Biol J Linn Soc 115:750–766CrossRefGoogle Scholar
  67. Lawson Handley LJ, 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
  68. Le Roux J, Wieczorek A (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17CrossRefGoogle Scholar
  69. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  70. Lee C, Gelembiuk G (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448PubMedPubMedCentralCrossRefGoogle Scholar
  71. Liebhold AM, Macdonald W, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci 41:1–49Google Scholar
  72. Liebhold AM, Brockerhoff EG, Garrett LJ, Parke JL, Britton KO (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Frontiers Ecol Environ 10:135–143CrossRefGoogle Scholar
  73. Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol Harlequin ladybird. PLoS ONE 5:e9743PubMedPubMedCentralCrossRefGoogle Scholar
  74. Loxdale H, Lushai G (2003) Rapid changes in clonal lines: the death of a ‘sacred cow’. Biol J Linn Soc 79:3–16CrossRefGoogle Scholar
  75. Lushai G, Loxdale HD, Allen JA (2003) The dynamic clonal genome and its adaptive potential. Biol J Linn Soc 79:193–208CrossRefGoogle Scholar
  76. Maddison DR, Guralnick R, Hill A, Reysenbach AL, McDade LA (2012) Ramping up biodiversity discovery via online quantum contributions. Trends Ecol Evol 27:72–77PubMedCrossRefGoogle Scholar
  77. Malacrida AR, Gomulski LM, Bonizzoni M, Bertin S, Gasperi G, Gugliclmino CR (2007) Globalization and fruitfly invasion and expansion: the medfly paradigm. Genetica 131:1–9PubMedCrossRefGoogle Scholar
  78. Mapondera TS, Burgess T, Matsuki M, Oberprieler RG (2012) Identification and molecular phylogenetics of the cryptic species of the Gonipterus scutellatus complex (Coleoptera: Curculionidae: Gonipterini). Aust J Entomol 51:175–188CrossRefGoogle Scholar
  79. Margaritopoulos JT, Kasprowicz L, Malloch GL, Fenton B (2009) Tracking the global dispersal of a cosmopolitan insect pest, the peach potato aphid. BMC Ecol 9:13PubMedPubMedCentralCrossRefGoogle Scholar
  80. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  81. Mendel Z, Protasov A, Fisher N, La Salle J (2004) Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Austral J Entomol 43:101–113CrossRefGoogle Scholar
  82. Miura O (2007) Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions. Ecol Res 22:876–883CrossRefGoogle Scholar
  83. Moran N (2007) Symbiosis as an adaptive process and source of phenotypic complexity. PNAS 104:8627–8633PubMedPubMedCentralCrossRefGoogle Scholar
  84. Mumford JD (2002) Economic issues related to quarantine in international trade. Eur Rev Agric Econ 29:329–348CrossRefGoogle Scholar
  85. Nadel R, Slippers B, Scholes M, Lawson S, Noack A, Wilcken C, Bouvet J, Wingfield MJ (2009) DNA bar-coding reveals source and patterns of Thaumastocoris peregrinus invasions in South Africa and South America. Biol Invasions 12:1067–1077CrossRefGoogle Scholar
  86. Nelson DR (2002) Current status of the Tardigrada: evolution and ecology. Integr Comp Biol 42:652–659PubMedCrossRefGoogle Scholar
  87. Nugnes F, Gebiola M, Monti MM, Gualtieri L, Giorgini M, Wang J, Bernardo U (2015) Genetic diversity of the invasive gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) and of its Rickettsia endosymbiont, and associated sex-ratio differences. PLoS ONE 10:e0124660PubMedPubMedCentralCrossRefGoogle Scholar
  88. Olatinwo R, Allison J, Meeker J, Johnson W, Streett D, Aime MC, Carlton C (2013) Detection and identification of Amylostereum areolatum (Russulales: Amylostereaceae) in the mycangia of Sirex nigricornis (Hymenoptera: Siricidae) in Central Louisiana. Environ Entomol 42:1246–1256PubMedCrossRefGoogle Scholar
  89. Paine TD, Jocelyn GM, Daane KM (2010) Accumulation of pest insects on Eucalyptus in California: random process or smoking gun? J Econom Entomol 103:1943–1949CrossRefGoogle Scholar
  90. Pamilo P (1988) Genetic variation in heterogeneous environments. Ann Zool Fenn 25:99–106Google Scholar
  91. Parker I, Simberloff D, Lonsdale W, Goodell K, Wonham M, Kareiva P, Williamson M, von Holle B, Moyle P, Byers J (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19CrossRefGoogle Scholar
  92. Pascual M, Chapuis MP, Mestres F, Balanya J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of Drosophila subobscura in the new world: a microsatellite-based survey using ABC methods. Mol Ecol 16:3069–3083PubMedCrossRefGoogle Scholar
  93. Peccoud J, Figueroa CC, Silva AX, Ramirez CC, Mieuzet L, Bonhomme J, Stoeckel S, Plantegenest M, Simon JC (2008) Host range expansion of an introduced insect pest through multiple colonizations of specialized clones. Mol Ecol 17:4608–4618PubMedCrossRefGoogle Scholar
  94. Pedersen JS, Krieger MJB, Vogel V, Giraud T, Keller L (2006) Native supercolonies of unrelated individuals in the invasive Argentine ant. Evolution 60:782–791PubMedCrossRefGoogle Scholar
  95. Perring TM (2001) The Bemisia tabaci species complex. Crop Protect 20:725–737CrossRefGoogle Scholar
  96. Petit R, Aguinagalde I, de Beaulieu J, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck G, Demesure-Musch B, Palme A, Martin J, Rendell S, Vendramin G (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565PubMedCrossRefGoogle Scholar
  97. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467PubMedCrossRefGoogle Scholar
  98. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  99. Pyšek P, Richardson D (2010) Invasive species, environmental change and management and health. Annu Rev Environ Resour 35:25–55CrossRefGoogle Scholar
  100. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242PubMedCrossRefGoogle Scholar
  101. Robert CP, Cornuet JM, Marin JM, Pillai NS (2011) Lack of confidence in approximate Bayesian computation model choice. Proc Natl Acad Sci USA 108:15112–15117PubMedPubMedCentralCrossRefGoogle Scholar
  102. Robertson A (1952) The effect of inbreeding on the variation due to recessive genes. Genetics 37:188–207Google Scholar
  103. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedCrossRefGoogle Scholar
  104. Roques A, Auger-Rozenberg MA, Blackburn TM, Garnas JR, Pyšek P, Rabitsch W, Richardson DM, Wingfield MJ, Liebhold AM, Duncan RP (2016) Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years. Biol Invasions. doi: 10.1007/s10530-016-1080-y
  105. Roy HE, Lawson Handley LJ (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248CrossRefGoogle Scholar
  106. Roy BA, Alexander HM, Davidson J, Campbell FT, Burdon JJ, Sniezko R, Brasier C (2014) Increasing forest loss worldwide from invasive pests requires new trade regulations. Front Ecol Environ 12:457–465CrossRefGoogle Scholar
  107. Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, De Clercq P, Comont RF, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar IA, Nedved O, Orlova-Bienkowskaja MJ, Rabitsch W,  Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre MG, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zakharov IA, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions. doi:  10.1007/s10530-016-1077-6
  108. Saccaggi DL, Karsten M, Robertson MP, Kumschick S, Somers MJ, Wilson JRU, Terblanche JS (2016) Methods and approaches for management of arthropod border incursions. Biol Invasions. doi: 10.1007/s10530-016-1085-6
  109. Saccheri IJ, Nichols RA, Brakefield PM (2006) Morphological differentiation following experimental bottlenecks in the butterfly Bicyclus anynana (Nymphalidae). Biol J Linn Soc 89:107–115CrossRefGoogle Scholar
  110. Sakai A, Allendorf F, Holt J, Lodge D, Molofsky J, Baughman S, Cabin R, Cohen J, Ellstrand N, McCauley D (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  111. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449PubMedPubMedCentralCrossRefGoogle Scholar
  112. Santana Q, Coetzee M, Steenkamp E, Mlonyeni O, Hammond G, Wingfield M, Wingfield B (2009) Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 46:217–223PubMedCrossRefGoogle Scholar
  113. Santini A, Ghelardini L, De Pace C, Desprez-Loustau M-L, Capretti P, Chandelier A, Cech T, Chira D, Diamandis S, Gaitniekis T, Hantula J, Holdenrieder O, Jankovsky L, Jung T, Jurc D, Kirisits T, Kunca A, Lygis V, Malecka M, Marcais B, Schmitz S, Schumacher J, Solheim H, Solla A, Szabò I, Tsopelas P, Vannini A, Vettraino AM, Webber J, Woodward S, Stenlid J (2013) Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol 197:238–250PubMedCrossRefGoogle Scholar
  114. Scaduto DA, Garner SR, Leach EL, Thompson AGJ (2012) Genetic evidence for multiple invasions of the Eastern Subterranean Termite into Canada. Environ Entomol 1:1680–1686CrossRefGoogle Scholar
  115. Shadmany M, Omar D, Muhamad R (2015) Biotype and insecticide resistance status of Bemisia tabaci populations from Peninsular Malaysia. J Appl Entomol 139:67–75CrossRefGoogle Scholar
  116. Skoracka A, Kuczyński L, Szydło W, Rector B (2013) The wheat curl mite Aceria tosichella (Acari: Eriophyidae) is a complex of cryptic lineages with divergent host ranges: evidence from molecular and plant bioassay data. Biol J Linn Soc 109:165–180CrossRefGoogle Scholar
  117. Skoracka A, Rector B, Kuczyński L, Szydło W, Hein G, French R (2014) Global spread of wheat curl mite by its most polyphagous and pestiferous lineages. Ann Appl Biol 165:222–235CrossRefGoogle Scholar
  118. Slippers B, Wingfield MJ, Coutinho TA, Wingfield BD (2001) Population structure and possible origin of Amylostereum areolatum in South Africa. Plant Pathol 50:206–210CrossRefGoogle Scholar
  119. Slippers B, Hurley BP, Wingfield MJ (2015) Sirex Woodwasp: a model for evolving management paradigms of invasive forest pests. Annu Rev Entomol 60:601–619PubMedCrossRefGoogle Scholar
  120. Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:3486–13491Google Scholar
  121. Spellerberg IF, Sawyer JWD (1999) Ecological patterns and types of species distribution. In: Spellerberg IF, Sawyer JWD (eds) An introduction to applied biogeography. Cambridge University Press, Cambridge, pp 108–133Google Scholar
  122. Starks P (2003) Selection for uniformity: xenophobia and invasion success. Trends Ecol Evol 18:159–162CrossRefGoogle Scholar
  123. Steiner WW (1977) Niche width and genetic variation in Hawaiian Drosophila. Am Nat 111:1037–1045CrossRefGoogle Scholar
  124. Taerum SJ, Duong TA, de Beer ZW, Gillette N, Sun J-H, Owen DR, Wingfield MJ (2013) Large shift in symbiont assemblage in the invasive Red Turpentine Beetle. PLoS ONE 8:e78126PubMedPubMedCentralCrossRefGoogle Scholar
  125. Tanaka K, Murata K, Matsuura A (2015) Rapid evolution of an introduced insect Ophraella communa LeSage in new environments: temporal changes and geographical differences in photoperiodic response. Entomol Sci 18:104–112CrossRefGoogle Scholar
  126. Tsutsui N, Suarez A, Grosberg R (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083PubMedPubMedCentralCrossRefGoogle Scholar
  127. Turgeon J, Tayeh A, Facon B, Lombaert E, De Clercq P, Berkvens N, Lundgren JG, Estoup A (2011) Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion. J Evol Biol 24:1044–1052PubMedCrossRefGoogle Scholar
  128. van Heerwaarden B, Willi Y, Kristensen TN, Hoffmann AA (2008) Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila. Genetics 179:2135–2146PubMedPubMedCentralCrossRefGoogle Scholar
  129. Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–390CrossRefGoogle Scholar
  130. Verhoeven KJF, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc R Soc Lond [Biol] 278:2–8CrossRefGoogle Scholar
  131. Vernot B, Akey JM (2014) Resurrecting surviving Neandertal lineages from modern human genomes. Science 343:1017–1021PubMedCrossRefGoogle Scholar
  132. Villablanca FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Mol Ecol 7:547–560PubMedCrossRefGoogle Scholar
  133. Vorburger C (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. J Evol Biol 19:97–107PubMedCrossRefGoogle Scholar
  134. Wares J, Hughes A, Grosberg R (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax D, Stachowitz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Sunderland, pp 229–257Google Scholar
  135. Wenger JA, Michel AP (2013) Implementing an evolutionary framework for understanding genetic relationships of phenotypically defined insect biotypes in the invasive soybean aphid (Aphis glycines). Evol Appl 6:1041–1053PubMedPubMedCentralGoogle Scholar
  136. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751PubMedCrossRefGoogle Scholar
  137. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580CrossRefGoogle Scholar
  138. Willis JH, Orr HA (1993) Increased heritable variation following population bottlenecks: the role of dominance. Evolution 47:949–957CrossRefGoogle Scholar
  139. Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144PubMedCrossRefGoogle Scholar
  140. Wingfield MJ, Garnas JR, Hajek A, Hurley BP, de Beer ZW, Taerum SJ (2016) Novel and co-evolved associations between insects and microorganisms as drivers of forest pestilence. Biol Invasions. doi: 10.1007/s10530-016-1084-7
  141. Wooding AL, Wingfield MJ, Hurley BP, Garnas JR, de Groot P, Slippers B (2013) Lack of fidelity revealed in an insect-fungal mutualism after invasion. Biol Lett 9:1–4CrossRefGoogle Scholar
  142. Zenni RD, Bailey JK, Simberloff D (2014) Rapid evolution and range expansion of an invasive plant are driven by provenance–environment interactions. Ecol Lett 17:727–735PubMedCrossRefGoogle Scholar
  143. Zepeda-Paulo FA, Simon JC, Ramirez CC, Fuentes-Contreras E, Margaritopoulos JT, Wilson ACC, Sorenson CE, Briones LM, Azevedo R, Ohashi DV, Lacroix C, Glais L, Figueroa CC (2010) The invasion route for an insect pest species: the tobacco aphid in the New World. Mol Ecol 19:4738–4752PubMedCrossRefGoogle Scholar
  144. Zielke DE, Werner D, Schaffner F, Kampen H, Fonseca DM (2014) Unexpected patterns of admixture in German populations of Aedes japonicus japonicus (Diptera: Culicidae) underscore the importance of human intervention. PLoS ONE 9:e99093PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Jeff R. Garnas
    • 1
    • 2
    Email author
  • Marie-Anne Auger-Rozenberg
    • 3
  • Alain Roques
    • 3
  • Cleo Bertelsmeier
    • 4
  • Michael J. Wingfield
    • 1
  • Davina L. Saccaggi
    • 5
  • Helen E. Roy
    • 6
  • Bernard Slippers
    • 1
    • 7
  1. 1.Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  2. 2.Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  3. 3.UR633, Zoologie ForestièreINRAOrléansFrance
  4. 4.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  5. 5.Plant Health Diagnostic Services, Department of AgricultureForestry and Fisheries (DAFF)StellenboschSouth Africa
  6. 6.NERC Centre for Ecology & HydrologyCrowmarsh Gifford, WallingfordUK
  7. 7.Department of GeneticsUniversity of PretoriaPretoriaSouth Africa

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