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Biological Invasions

, Volume 18, Issue 1, pp 31–44 | Cite as

Reconstructing the invasion history of the lily leaf beetle, Lilioceris lilii, in North America

  • Alessandro Dieni
  • Jacques Brodeur
  • Julie Turgeon
Original Paper

Abstract

Identifying routes of invasions of exotic organisms is an essential step to prevent further introductions and to manage established populations. The invasion of North America by the lily leaf beetle (Lilioceris lilii) is well documented, but the source(s) of the introduced population(s) and the geographical pathway(s) followed by the beetle during its progression in North America remain unknown. We used amplified fragment length polymorphism to characterize the genotype of 516 individuals across 25 locations in North America and 9 locations in Europe. Genetic clustering analyses and principal coordinate analyses revealed clear genetic differences between individuals from Canada and the USA, suggesting two different episodes of introduction in North America, a first one in Montréal, QC, Canada, in 1943 and a second one in Cambridge, Massachusetts, United States of America, in 1992. Population allocation analyses further suggested that the invasive populations of L. lilii originated from northern Europe, probably in southern United Kingdom and the western part of Germany. Finally, dates of first mentions of the beetle across North America, paired with the genetic diversity of the beetles at each location, showed that there are two separate routes of invasion of L. lilii with distinctive patterns of dispersal.

Keywords

Lily leaf beetle Lilioceris lilii Invasive species Routes of invasion AFLP Populations genetic 

Notes

Acknowledgments

We thank Josée Doyon, Alexandra Saad and Alexandre Leblanc for their help in the field; Audrey Bourret, Geneviève Parent, Éric Devost and Xavier Prairie for technical assistance in the laboratory; and all lily leaf beetles collectors who kindly provided samples from across Europe and North America. The Canada Research Chair in Biological Control provided financial support to this project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2015_987_MOESM1_ESM.pdf (197 kb)
Supplementary material 1 (PDF 196 kb)
10530_2015_987_MOESM2_ESM.pdf (82 kb)
Supplementary material 2 (PDF 82 kb)
10530_2015_987_MOESM3_ESM.pdf (445 kb)
Supplementary material 3 (PDF 444 kb)

References

  1. Alda F, Ruiz-López MJ, García FJ, Gompper ME, Eggert LS, García JT (2013) Genetic evidence for multiple introduction events of raccoons (Procyon lotor) in Spain. Biol Invasions 15:687–698CrossRefGoogle Scholar
  2. Audisio P (2011) Fauna Europaea: Lilioceris lilii. In: Fauna Europaea version 2.4. http://www.faunaeur.org/full_results.php?id=243537. Accessed 11 May 2012
  3. Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD-genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species; the American lobster (Homarus americanus). Mol Ecol 24:3299–3315PubMedCrossRefGoogle Scholar
  4. Berti N, Rapilly M (1976) Liste d’espèces et révision du genre Lilioceris Reitter (Col. Chrysomelidae). In: Faune d’Iran. Annales de la Société Entomologique de France (Nouvelle série), France, pp 31–73Google Scholar
  5. Boissin E, Hurley B, Wingfield M, Vasaitis R, Stenlid J, Davis C, Groot PD, Ahumada R, Carnegie A, Goldarazena A (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744PubMedCrossRefGoogle Scholar
  6. Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273PubMedCrossRefGoogle Scholar
  7. Bouchard AM, McNeil JN, Brodeur J (2008) Invasion of American native lily populations by an alien beetle. Biol Invasions 10:1365–1372CrossRefGoogle Scholar
  8. Buschman J (2004) Globalisation-flower–flower bulbs–bulb flowers. IX Int Symp Flower Bulbs 673:27–33Google Scholar
  9. Ciosi M, Miller N, Kim K, 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
  10. Colbeck GJ, Turgeon J, Sirois P, Dodson JJ (2011) Historical introgression and the role of selective vs. neutral processes in structuring nuclear genetic variation (AFLP) in a circumpolar marine fish, the capelin (Mallotus villosus). Mol Ecol 20:1976–1987PubMedCrossRefGoogle Scholar
  11. Darling JA, Bagley MJ, Roman J, Tepolt CK, Geller JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007PubMedCrossRefGoogle Scholar
  12. Day R (1993) Lilioceris lilii. A report to E.O. Stockbridge, OIC. APHIS, 10 Causeway St., Boston, MA, USAGoogle Scholar
  13. Dlugosch K, Parker I (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  14. Donovan GH, Butry DT, Michael YL, Prestemon JP, Liebhold AM, Gatziolis D, Mao MY (2013) The relationship between trees and human health: evidence from the spread of the emerald ash borer. Am J Prev Med 44:139–145PubMedCrossRefGoogle Scholar
  15. Duchesne P, Bernatchez L (2002) AFLPOP: a computer program for simulated and real population allocation, based on AFLP data. Mol Ecol Notes 2:380–383CrossRefGoogle Scholar
  16. Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  17. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130PubMedCrossRefGoogle Scholar
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47PubMedCentralGoogle Scholar
  20. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedPubMedCentralCrossRefGoogle Scholar
  21. Guillemaud T, Beaumont MA, Ciosi M, Cornuet J-M, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99PubMedCrossRefGoogle Scholar
  22. Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns, and processes. Biol Control 35:227–239CrossRefGoogle Scholar
  23. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  24. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6: 13. v.3.23 http://ibdws.sdsu.edu
  25. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94PubMedPubMedCentralCrossRefGoogle Scholar
  26. Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632PubMedPubMedCentralCrossRefGoogle Scholar
  27. Kang M, Buckley YM, Lowe AJ (2007) Testing the role of genetic factors across multiple independent invasions of the shrub Scotch broom (Cytisus scoparius). Mol Ecol 16:4662–4673PubMedCrossRefGoogle Scholar
  28. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  29. Labeyrie V (1963) Lilioceris. In: Balachowsky AS (ed) In Entomologie Appliquée à l’Agriculture, Tome 1. Masson and Cie, Paris, pp 588–595Google Scholar
  30. LeSage L (1983) Note sur la distribution présente et future du criocère du lys, Lilioceris lilii Scopoli (Coleoptera: Chrysomelidae), dans l’est du Canada. Le Nat Can 110:95–97Google Scholar
  31. LeSage L, Elliott B (2003) Major range extension of the lily leaf beetle (Coleoptera: Chrysomelidae), a pest of wild and cultivated Liliaceae. Can Entomol 135:587–588CrossRefGoogle Scholar
  32. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408PubMedCrossRefGoogle Scholar
  33. Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B, Grez A, Loomans A, Malausa T, Nedved O, Rhule E (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23:5979–5997PubMedCrossRefGoogle Scholar
  34. Mack RN, Simberloff D, Lonsdale MW, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  35. Majka CG, Kirby C (2011) Lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae), in Maine and the Maritime Provinces: the continuing dispersal of an invasive species. J Acad Entomol Soc 7:70–74Google Scholar
  36. Majka CG, LeSage L (2008) Introduced leaf beetles of the maritime provinces, 5: The lily leaf beetle, Lilioceris Lilii (Scopoli) (Coleoptera: Chrysomelidae). Proc Entomol Soc Wash 110:186–195CrossRefGoogle Scholar
  37. Marrs R, Sforza R, Hufbauer R (2008) Evidence for multiple introductions of Centaurea stoebe micranthos (spotted knapweed, Asteraceae) to North America. Mol Ecol 17:4197–4208PubMedCrossRefGoogle Scholar
  38. McFadden MW, McManus ME (1991) An insect out of control? The potential for spread and establishment of the gypsy moth in new forest areas in the United States. In: Baranchikov YN, Mattson WJ, Hain FP, Payne TL (eds) Forest insect guilds: patterns of interaction with host trees. U.S. Forest Service General Technical Report NE-153Google Scholar
  39. Orlóci L (1978) Multivariate analysis in vegetation research. Junk, The HagueGoogle Scholar
  40. Orlova-Bienkowskaja MJ (2013) Dynamics of the range of lily leaf beetle (Lilioceris lilii, Chrysomelidae, Coleoptera) indicates its invasion from Asia to Europe in the 16th–17th century. Rus J Biol Invasions 4:93–104CrossRefGoogle Scholar
  41. Pascual M, Chapuis M, Mestres F, Balanya J, Huey R, Gilchrist G, 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
  42. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  43. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedPubMedCentralCrossRefGoogle Scholar
  44. Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504PubMedCrossRefGoogle Scholar
  45. Pelletier TA, Carstens BC (2014) Model choice for phylogeographic inference using a large set of models. Mol Ecol 23:3028–3043PubMedCrossRefGoogle Scholar
  46. Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’connell C, Wong E, Russel L, Zern J, Aquino T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20CrossRefGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  48. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  49. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  50. Rollins LA, Woolnough AP, Wilton AN, Sinclair R, Sherwin WB (2009) Invasive species can’t cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol Ecol 18:1560–1573PubMedCrossRefGoogle Scholar
  51. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  52. Rosenthal DM, Ramakrishnan AP, Cruzan MB (2008) Evidence for multiple sources of invasion and intraspecific hybridization in Brachypodium sylvaticum (Hudson) Beauv. in North America. Mol Ecol 17:4657–4669PubMedCrossRefGoogle Scholar
  53. Shirk R, Hamrick J, Zhang C, Qiang S (2014) Patterns of genetic diversity reveal multiple introductions and recurrent founder effects during range expansion in invasive populations of Geranium carolinianum (Geraniaceae). Heredity 112:497–507PubMedPubMedCentralCrossRefGoogle Scholar
  54. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100PubMedPubMedCentralCrossRefGoogle Scholar
  55. Tatem AJ, Hay SI, Rogers DJ (2006) Global traffic and disease vector dispersal. Proc Natl Acad Sci USA 103:6242–6247PubMedPubMedCentralCrossRefGoogle Scholar
  56. Tepolt C, Darling J, Bagley M, Geller J, Blum M, Grosholz E (2009) European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population. Divers Distrib 15:997–1009CrossRefGoogle Scholar
  57. Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151PubMedCrossRefGoogle Scholar
  58. Waage J (1990) Ecological theory and the selection of biological control agents. In: Mackauer M, Ehler IE, Roland J (eds) In Critical issues in biological control. Intercept, Andover, pp 135–157Google Scholar
  59. Whitmire SL, Tobin PC (2006) Persistence of invading gypsy moth populations in the United States. Oecologia 147:230–237PubMedCrossRefGoogle Scholar
  60. Yu P, Lu W, Casagrande RA (2001) Lilioceris lilii (Scopoli) occurs in China (Coleoptera: Chrysomelidae). Coleopts Bull 55:65–66CrossRefGoogle Scholar
  61. Zhang YY, Zhang DY, Barrett SC (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol Ecol 19:1774–1786PubMedCrossRefGoogle Scholar
  62. Zhang B, Edwards O, Kang L, Fuller S (2014) A multi-genome analysis approach enables tracking of the invasion of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World. Mol Ecol 23:1940–1951PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Alessandro Dieni
    • 1
  • Jacques Brodeur
    • 1
  • Julie Turgeon
    • 2
  1. 1.Institut de Recherche en Biologie VégétaleUniversité de MontréalMontrealCanada
  2. 2.Département de BiologieUniversité LavalQuébecCanada

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