Biological Invasions

, Volume 20, Issue 3, pp 665–677 | Cite as

Colonization history of the western corn rootworm (Diabrotica virgifera virgifera) in North America: insights from random forest ABC using microsatellite data

  • Eric Lombaert
  • Marc Ciosi
  • Nicholas J. Miller
  • Thomas W. Sappington
  • Aurélie Blin
  • Thomas Guillemaud
Original Paper


First described from western Kansas, USA, the western corn rootworm, Diabrotica virgifera virgifera, is one of the worst pests of maize. The species is generally thought to be of Mexican origin and to have incidentally followed the expansion of maize cultivation into North America thousands of years ago. However, this hypothesis has never been investigated formally. In this study, the genetic variability of samples collected throughout North America was analysed at 13 microsatellite marker loci to explore precisely the population genetic structure and colonization history of D. v. virgifera. In particular, we used up-to-date approximate Bayesian computation methods based on random forest algorithms to test a Mexican versus a central-USA origin of the species, and to compare various possible timings of colonization. This analysis provided strong evidence that the origin of D. v. virgifera was southern (Mexico, or even further south). Surprisingly, we also found that the expansion of the species north of its origin was recent—probably not before 1100 years ago—thus indicating it was not directly associated with the early history of maize expansion out of Mexico, a far more ancient event.


Biological invasion Invasion routes Approximate Bayesian computation Maize 



We thank our colleagues Rosanna Giordano, Stephan Toepfer, Uwe Stoltz, Kyung Seok Kim, Sue Ratcliff, Greg Cronholm, Lee French, Lance Meinke, Brendon Reardon, Eli Levine, Bruce Eisley, Dennis Calvin, Joanne Whalen and Ken Wise for D. v. virgifera beetles and DNA samples. We also thank Emeline Deleury, Arnaud Estoup and Andrea Benazzo for scripts to compute summary statistics. We also thank Alexandra Auguste, Paulette Flacchi and Marie-José Odonne for technical and administrative assistance. This work was funded by grants from ANR projects Bioinv4I and Emile, and from the French Agropolis Fondation (Labex Agro-Montpellier, BIOFIS).

Author contributions

EL and TG designed the study. TS managed the collection of samples. MC, NM and AB genotyped the samples. EL and TG analysed the data. EL, MC, NM, TS and TG wrote the paper. All authors have revised and approved the final manuscript.

Supplementary material

10530_2017_1566_MOESM1_ESM.pdf (973 kb)
Supplementary material 1 (PDF 972 kb)


  1. Anderson E, Brown WL (1952) The history of the common maize varieties of the United States Corn Belt. Agric Hist 26:2–8Google Scholar
  2. Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035PubMedPubMedCentralGoogle Scholar
  3. Benazzo A, Ghirotto S, Vilaça ST, Hoban S (2015) Using ABC and microsatellite data to detect multiple introductions of invasive species from a single source. Heredity (Edinb) 115:262–272. doi: 10.1038/hdy.2015.38 CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300Google Scholar
  5. Bermond G, Ciosi M, Lombaert E et al (2012) Secondary contact and admixture between independently invading populations of the Western Corn Rootworm, Diabrotica virgifera virgifera in Europe. PLoS ONE 7:12. doi: 10.1371/journal.pone.0050129 CrossRefGoogle Scholar
  6. Bermond G, Blin A, Vercken E et al (2013) Estimation of the dispersal of a major pest of maize by cline analysis of a temporary contact zone between two invasive outbreaks. Mol Ecol 22:5368–5381. doi: 10.1111/mec.12489 CrossRefPubMedGoogle Scholar
  7. Boyd M, Varney T, Surette C, Surette J (2008) Reassessing the northern limit of maize consumption in North America: stable isotope, plant microfossil, and trace element content of carbonized food residue. J Archaeol Sci 35:2545–2556. doi: 10.1016/j.jas.2008.04.008 CrossRefGoogle Scholar
  8. Branson TF, Krysan JL (1981) Feeding and oviposition behavior and life cycle strategies of Diabrotica: an evolutionary view with implications for pest management. Environ Entomol 10:826–831CrossRefGoogle Scholar
  9. Breiman L (2001) Random forests. Mach Learn 45:5–32. doi: 10.1023/A:1010933404324 CrossRefGoogle Scholar
  10. Buckler ES, Stevens NM (2006) Maize origins, domestication, and selection. In: Motley TJ, Zerega N, Cross H (eds) Darwin’s Harvest: new approaches to the origins, evolution, and conservation of crops, 1st edn. Columbia University Press, pp 67–90Google Scholar
  11. Campbell LA, Meinke LJ (2006) Seasonality and adult habitat use by four Diabrotica species at prairie-corn interfaces. Environ Entomol 35:922–936. doi: 10.1603/0046-225x-35.4.922 CrossRefGoogle Scholar
  12. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis models and estimation procedures. Am J Hum Genet 19:233–257PubMedPubMedCentralGoogle Scholar
  13. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi: 10.1093/molbev/msl191 CrossRefPubMedGoogle Scholar
  14. Chiang HC (1973) Bionomics of the northern and western corn rootworms. Annu Rev Entomol 18:47–72CrossRefGoogle Scholar
  15. Choisy M, Franck P, Cornuet JM (2004) Estimating admixture proportions with microsatellites: comparison of methods based on simulated data. Mol Ecol 13:955–968. doi: 10.1111/j.1365-294X.2004.02107.x CrossRefPubMedGoogle Scholar
  16. Ciosi M, Miller NJ, Kim KS et al (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. doi: 10.1111/j.1365-294X.2008.03866.x CrossRefPubMedGoogle Scholar
  17. Clark TL, Hibbard BE (2004) Comparison of nonmaize hosts to support western corn rootworm (Coleoptera: Chrysomelidae) larval biology. Environ Entomol 33:681–689CrossRefGoogle Scholar
  18. Coates BS, Sumerford DV, Miller NJ et al (2009) Comparative performance of single nucleotide polymorphism and microsatellite markers for population genetic analysis. J Hered 100:556–564. doi: 10.1093/jhered/esp028 CrossRefPubMedGoogle Scholar
  19. Coats SA, Tollefson JJ, Mutchmor JA (1986) Study of migratory flight in the western corn-rootworm (coleoptera, chrysomelidae). Environ Entomol 15:620–625. doi: 10.1093/ee/15.3.620 CrossRefGoogle Scholar
  20. Coltrain JB, Janetski JC, Carlyle SW (2010) The stable- and radio-isotope chemistry of western basketmaker burials: implications for early puebloan diets and origins. Am Archaeol 72:301–321Google Scholar
  21. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedPubMedCentralGoogle Scholar
  22. Cornuet JM, Santos F, Beaumont MA et al (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719. doi: 10.1093/bioinformatics/btn514 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cornuet J-M, Pudlo P, Veyssier J et al (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism. DNA sequence and microsatellite data. Bioinformatics 30:1187–1189. doi: 10.1093/bioinformatics/btt763 CrossRefPubMedGoogle Scholar
  24. Coulon A, Fitzpatrick JW, Bowman R et al (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701. doi: 10.1111/j.1365-294X.2008.03705.x CrossRefPubMedGoogle Scholar
  25. da Fonseca RR, Smith BD, Wales N et al (2015) The origin and evolution of maize in the Southwestern United States. Nat Plants 1:14003. doi: 10.1038/nplants.2014.3 CrossRefPubMedGoogle Scholar
  26. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B Methodol 39:1–38. doi: 10.2307/2984875 Google Scholar
  27. Doebley J, Wendel JD, Smith JSC et al (1988) The origin of cornbelt maize: the isozyme evidence. Econ Bot 42:120–131. doi: 10.1007/BF02859042 CrossRefGoogle Scholar
  28. Estoup A, Lombaert E, Marin JM et al (2012) Estimation of demo-genetic model probabilities with Approximate Bayesian computation using linear discriminant analysis on summary statistics. Mol Ecol Resour 12:846–855. doi: 10.1111/j.1755-0998.2012.03153.x CrossRefPubMedGoogle Scholar
  29. 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. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  30. 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. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  31. Excoffier L, Dupanloup I, Huerta-Sánchez E et al (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905. doi: 10.1371/journal.pgen.1003905 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fraimout A, Debat V, Fellous S et al (2017) Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Mol Biol Evol 34:980–996. doi: 10.1093/molbev/msx050 PubMedPubMedCentralGoogle Scholar
  33. Fritz G (1990) Multiple pathways to farming in precontact North America. J World Prehistory 4:387–435CrossRefGoogle Scholar
  34. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  35. Gillette CP (1912) Diabrotica virgifera Le Conte as a corn rootworm. J Econ Entomol 5:364–366CrossRefGoogle Scholar
  36. Grant RH, Seevers KP (1989) Local and long-range movement of adult western corn-rootworm (Coleoptera, Chrysomelidae) as evidenced by washup along southern Lake-Michigan shores. Environ Entomol 18:266–272CrossRefGoogle Scholar
  37. Gray ME, Sappington TW, Miller NJ et al (2009) Adaptation and Invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu Rev Entomol 54:303–321CrossRefPubMedGoogle Scholar
  38. Hallatschek O, Nelson DR (2008) Gene surfing in expanding populations. Theor Popul Biol 73:158–170. doi: 10.1016/j.tpb.2007.08.008 CrossRefPubMedGoogle Scholar
  39. Hart JP, Brumbach HJ, Lusteck R (2007) Extending the phytolith evidence for early maize (Zea mays ssp. mays) and squash (Cucurbita sp.) in central New York. Am Antiq 72:563–583CrossRefGoogle Scholar
  40. Horn GH (1893) The galerucini of Boreal America. Trans Am Entomol Soc 20:57–136Google Scholar
  41. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi: 10.1111/j.1471-8286.2004.00845.x CrossRefGoogle Scholar
  42. Kim KS, Sappington TW (2005) Genetic structuring of western corn rootworm (Coleoptera: Chrysomelidae) populations in the United States based on microsatellite loci analysis. Environ Entomol 34:494–503CrossRefGoogle Scholar
  43. Kim KS, Ratcliffe ST, French BW et al (2008) Utility of EST-Derived SSRs as population genetics markers in a beetle. J Hered 99:112–124. doi: 10.1093/jhered/esm104 CrossRefPubMedGoogle Scholar
  44. Krysan JL, Smith RF (1987) Systematics of the virgifera species group of Diabrotica (Coleoptera: Chrysomelidae: Galerucinae). Entomography 5:375–484Google Scholar
  45. Kutka F (2011) Open-pollinated vs. hybrid maize cultivars. Sustainability 3:1531–1554. doi: 10.3390/su3091531 Google Scholar
  46. Langella O (1999) Populations 1.2.32 (02/13/2011): a population genetic softwareGoogle Scholar
  47. Le Conte JL (1868) New Coleoptera collected on the survey for the extension of the Union Pacific Railway, E. D. from Kansas to Fort Craig, New Mexico. Trans Am Entomol Soc 2:49–59Google Scholar
  48. Le Corre V, Kremer A (1998) Cumulative effects of founding events during colonisation on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11:495–512. doi: 10.1007/s000360050102 CrossRefGoogle Scholar
  49. Levine E, Oloumi-Sadeghi H (1991) Management of diabroticite rootworms in corn. Annu Rev Entomol 36:229–255. doi: 10.1146/annurev.ento.36.1.229 CrossRefGoogle Scholar
  50. Lombaert E, Guillemaud T, Thomas CE et al (2011) Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Mol Ecol 20:4654–4670. doi: 10.1111/j.1365-294X.2011.05322.x CrossRefPubMedGoogle Scholar
  51. Lombaert E, Guillemaud T, Lundgren J et al (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23:5979–5997. doi: 10.1111/mec.12989 CrossRefPubMedGoogle Scholar
  52. Matsuoka Y, Vigouroux Y, Goodman MM et al (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084. doi: 10.1073/pnas.052125199 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Meinke LJ, Sappington TW, Onstad DW et al (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric For Entomol 11:29–46. doi: 10.1111/j.1461-9563.2008.00419.x CrossRefGoogle Scholar
  54. Merrill WL, Hard RJ, Mabry JB et al (2009) The diffusion of maize to the southwestern United States and its impact. Proc Natl Acad Sci USA 106:21019–21026. doi: 10.1073/pnas.0906075106 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Metcalf RL (1983) Implications and prognosis of resistance to insecticides. In: Georghiou GP, Saito T (eds) Pest resistance to pesticides, 1st edn. Plenum Press, New York and London, pp 703–733CrossRefGoogle Scholar
  56. Metcalf RL (1986) The ecology of insecticides and the chemical control of insects. In: Kogan M (ed) Ecological theory and integrated pest management practice. Wiley, New York, pp 251–297Google Scholar
  57. Metcalf RL, Lampman RL (1989) The chemical ecology of diabroticites and cucurbitaceae. Experientia 45:240–247CrossRefGoogle Scholar
  58. Miller N, Estoup A, Toepfer S et al (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992. doi: 10.1126/science.1115871 CrossRefPubMedGoogle Scholar
  59. Moeser J, Hibbard BE (2005) A synopsis of the nutritional ecology of larvae and adults of Diabrotica virgifera virgifera (LeConte) in the new and old world—nouvelle cuisine for the invasive maize pest Diabrotica virgifera virgifera in Europe? In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management, 1st edn. Cabi Publishing, pp 41–65Google Scholar
  60. Momigliano P, Jokinen H, Fraimout A et al (2017) Extraordinarily rapid speciation in a marine fish. Proc Natl Acad Sci 114:6074–6079. doi: 10.1073/pnas.1615109114 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  62. Oyediran IO, Hibbard BE, Clark TL (2004) Prairie grasses as hosts of the western corn rootworm (Coleoptera: Chrysomelidae). Environ Entomol 33:740–747. doi: 10.1603/0046-225X-33.3.740 CrossRefGoogle Scholar
  63. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855. doi: 10.1046/j.1523-1739.1998.96489.x CrossRefGoogle Scholar
  64. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  65. Pudlo P, Marin JM, Estoup A et al (2016) Reliable ABC model choice via random forests. Bioinformatics 32:859–866. doi: 10.1093/bioinformatics/btv684 CrossRefPubMedGoogle Scholar
  66. Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4:4399–4428. doi: 10.1002/ece3.1305 PubMedPubMedCentralGoogle Scholar
  67. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201CrossRefPubMedPubMedCentralGoogle Scholar
  68. Raymond M, Rousset F (1995) Genepop (version. 1.2), a population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  69. Raynal L, Marin J-M, Pudlo P, et al (2017) ABC random forests for Bayesian parameter inference. arXiv:1605.05537Google Scholar
  70. Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  71. Simon ML (2017) Reevaluating the Evidence for Middle Woodland Maize From the Holding Site. Am Antiq 82:140–150. doi: 10.1017/aaq.2016.2 CrossRefGoogle Scholar
  72. Smith RF (1966) Distributional patterns of selected western north American insects: the distribution of Diabroticites in western north America. Bull Entomol Soc Am 12:108–110Google Scholar
  73. Smith B (2017) Tracing the initial diffusion of maize in North America. In: Boivin N, Petraglia M, Crassard R (eds) From colonisation to globalisation: species movements in human history, 1st edn. Cambridge University Press, Cambridge, pp 332–348Google Scholar
  74. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Google Scholar
  75. Tenaillon MI, Charcosset A (2011) A European perspective on maize history. C R Biol 334:221–228. doi: 10.1016/j.crvi.2010.12.015 CrossRefPubMedGoogle Scholar
  76. Vilà M, Basnou C, Gollasch S et al (2009) One hundred of the most invasive alien species in Europe. In: DAISIE (Delivering Alien Invasive Species Inventories for Europe) (ed) Handbook of alien species Europe, Springer, Netherlands, pp 265–268CrossRefGoogle Scholar
  77. Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L (2010) ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinform 11:7. doi: 10.1186/1471-2105-11-116 CrossRefGoogle Scholar
  78. Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution (NY) 38:1358–1370Google Scholar
  79. Youngman RR, Day ER (1993) Incidence of western corn rootworm beetles (Coleoptera, Chrysomelidae) on corn in Virginia from 1987 to 1992. J Entomol Sci 28:136–141CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Université Côte d’Azur, INRA, CNRSISASophia Antipolis CedexFrance
  2. 2.Institute of Molecular Cell and Systems BiologyUniversity of GlasgowGlasgowUK
  3. 3.Department of BiologyIllinois Institute of TechnologyChicagoUSA
  4. 4.USDA-Agricultural Research Service, Corn Insects and Crop Genetics Research Unit, Genetics LaboratoryIowa State UniversityAmesUSA

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