Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 15:687–698

    Article  Google Scholar 

  • 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

  • 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 24:3299–3315

    Article  PubMed  Google Scholar 

  • 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 31–73

  • 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 21:5728–5744

    Article  PubMed  CAS  Google Scholar 

  • 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 13:3261–3273

    Article  PubMed  CAS  Google Scholar 

  • Bouchard AM, McNeil JN, Brodeur J (2008) Invasion of American native lily populations by an alien beetle. Biol Invasions 10:1365–1372

    Article  Google Scholar 

  • Buschman J (2004) Globalisation-flower–flower bulbs–bulb flowers. IX Int Symp Flower Bulbs 673:27–33

    Google Scholar 

  • 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 17:3614–3627

    Article  PubMed  CAS  Google Scholar 

  • 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 20:1976–1987

    Article  PubMed  Google Scholar 

  • 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 17:4992–5007

    Article  PubMed  CAS  Google Scholar 

  • Day R (1993) Lilioceris lilii. A report to E.O. Stockbridge, OIC. APHIS, 10 Causeway St., Boston, MA, USA

  • Dlugosch K, Parker I (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 

  • 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 44:139–145

    Article  PubMed  Google Scholar 

  • Duchesne P, Bernatchez L (2002) AFLPOP: a computer program for simulated and real population allocation, based on AFLP data. Mol Ecol Notes 2:380–383

    Article  CAS  Google Scholar 

  • Earl DA (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 

  • 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  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47

    PubMed Central  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 104:88–99

    Article  PubMed  CAS  Google Scholar 

  • Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns, and processes. Biol Control 35:227–239

    Article  Google Scholar 

  • 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 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6: 13. v.3.23 http://ibdws.sdsu.edu

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 106:625–632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 16:4662–4673

    Article  PubMed  CAS  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  PubMed  CAS  Google Scholar 

  • Labeyrie V (1963) Lilioceris. In: Balachowsky AS (ed) In Entomologie Appliquée à l’Agriculture, Tome 1. Masson and Cie, Paris, pp 588–595

    Google Scholar 

  • 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 110:95–97

    Google Scholar 

  • LeSage L, Elliott B (2003) Major range extension of the lily leaf beetle (Coleoptera: Chrysomelidae), a pest of wild and cultivated Liliaceae. Can Entomol 135:587–588

    Article  Google Scholar 

  • Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408

    Article  PubMed  CAS  Google Scholar 

  • 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 23:5979–5997

    Article  PubMed  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale MW, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • 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 7:70–74

    Google Scholar 

  • 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 110:186–195

    Article  Google Scholar 

  • Marrs R, Sforza R, Hufbauer R (2008) Evidence for multiple introductions of Centaurea stoebe micranthos (spotted knapweed, Asteraceae) to North America. Mol Ecol 17:4197–4208

    Article  PubMed  CAS  Google Scholar 

  • 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-153

  • Orlóci L (1978) Multivariate analysis in vegetation research. Junk, The Hague

    Google Scholar 

  • 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 4:93–104

    Article  Google Scholar 

  • 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 16:3069–3083

    Article  PubMed  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  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 

  • Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504

    Article  PubMed  Google Scholar 

  • Pelletier TA, Carstens BC (2014) Model choice for phylogeographic inference using a large set of models. Mol Ecol 23:3028–3043

    Article  PubMed  Google Scholar 

  • 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 84:1–20

    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 

  • 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/

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • 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 18:1560–1573

    Article  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • 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 17:4657–4669

    Article  PubMed  Google Scholar 

  • 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 112:497–507

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 98:1095–1100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tatem AJ, Hay SI, Rogers DJ (2006) Global traffic and disease vector dispersal. Proc Natl Acad Sci USA 103:6242–6247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 15:997–1009

    Article  Google Scholar 

  • 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 11:139–151

    Article  PubMed  CAS  Google Scholar 

  • 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 135–157

    Google Scholar 

  • Whitmire SL, Tobin PC (2006) Persistence of invading gypsy moth populations in the United States. Oecologia 147:230–237

    Article  PubMed  Google Scholar 

  • Yu P, Lu W, Casagrande RA (2001) Lilioceris lilii (Scopoli) occurs in China (Coleoptera: Chrysomelidae). Coleopts Bull 55:65–66

    Article  Google Scholar 

  • Zhang YY, Zhang DY, Barrett SC (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol Ecol 19:1774–1786

    Article  PubMed  CAS  Google Scholar 

  • 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 23:1940–1951

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandro Dieni.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dieni, A., Brodeur, J. & Turgeon, J. Reconstructing the invasion history of the lily leaf beetle, Lilioceris lilii, in North America. Biol Invasions 18, 31–44 (2016). https://doi.org/10.1007/s10530-015-0987-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0987-z

Keywords

Navigation