Biological Invasions

, Volume 11, Issue 2, pp 299–314 | Cite as

Tracing the invasion history of mealy plum aphid, Hyalopterus pruni (Hemiptera: Aphididae), in North America: a population genetics approach

  • Jeffrey D. Lozier
  • George K. Roderick
  • Nicholas J. Mills
Original Paper


Biological invasions are typically the outcome of complex patterns of introduction, establishment, and spread, and genetic methods are excellent tools to resolve such histories for non-native organisms. The mealy plum aphid, Hyalopterus pruni, is an invasive pest of dried plum in California. We examined nine microsatellite loci and DNA sequences from three mitochondrial genes (1,148 bp) in populations throughout the native and invaded ranges of H. pruni to assess key invasion parameters, including geographic origins of invasive populations, number of introductions, and levels of genetic diversity and gene flow. Our results provide evidence for multiple invasions of H. pruni into North America, suggesting that aphids in California may have been introduced from Spain, and aphids in the eastern United States and Vancouver, Canada were likely introduced from central or northern Europe. H. pruni populations in California were characterized by low genetic diversity relative to native populations, while the two other North American populations were less genetically impoverished. Gene flow among introduced populations was low, but does appear to occur with some regularity. These findings provide a framework for more detailed studies of H. pruni, but also represent a model for how population genetics approaches can be used to study invasion biology and aid the development of optimized management methods for agricultural pests.


Hyalopterus Aphids Invasion genetics Microsatellites Mitochondrial DNA Population bottlenecks 



The authors gratefully recognize funding support from the EPA STAR program, the UC IPM Exotic Pest and Disease Research Program, USDA NRI, and the University of California Agriculture Experiment Station. We also thank our numerous collaborators (Table 1) for providing Hyalopterus specimens, Per Palsbøll for developing and providing the software for Kst estimation, and two anonymous reviewers and Margarita Hadjistylli for helpful comments. This work was completed as part of J Lozier’s doctoral dissertation.

Supplementary material

10530_2008_9248_MOESM1_ESM.doc (372 kb)
(DOC 371 kb)
10530_2008_9248_MOESM2_ESM.doc (194 kb)
(DOC 104 kb)


  1. Bellows TS (2001) Restoring population balance through natural enemy introductions. Biol Control 21:199–205CrossRefGoogle Scholar
  2. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedGoogle Scholar
  3. Clement M, Posada D, Crandall K (2000) TCS: A computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  4. Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000PubMedGoogle Scholar
  5. Crooks JA, Soulé ME (1999) Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei PJ, Viken Å (eds) Invasive species and biodiversity management. Kluwer Academic Publishers, The Netherlands, pp 103–125Google Scholar
  6. Davies N, Villablanca FX, Roderick GK (1999) Determining the sources of individuals in recently founded populations: multilocus genotyping in non-equilibrium genetics. Trends Ecol Evol 14:17–21PubMedCrossRefGoogle Scholar
  7. Delmotte F, Leterme N, Gauthier J-P, Rispe C, Simon J-C (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Mol Ecol 11:711–723PubMedCrossRefGoogle Scholar
  8. di Castri F (1989) History of biological invasions with special emphasis on the old world. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. Wiley, New York, pp 1–30Google Scholar
  9. Dixon AFG (1998) Aphid ecology, 2nd edn. Chapman and Hall, LondonGoogle Scholar
  10. Dunmire WW (2004) Gardens of New Spain: how Mediterranean plants and foods changed America. University of Texas Press, AustinGoogle Scholar
  11. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  12. Felsenstein J (2002) PHYLIP (Phylogeny Inference Package) version 3.6a3. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  13. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indeces (version 2.9.3).
  14. Hood GM (2006) PopTools—Software for the Analysis of Ecological Models. Version 2.7.
  15. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151PubMedGoogle Scholar
  16. Hufbauer RA, Roderick GK (2005) Microevolution in biological control: Mechanisms, patterns, and process. Biol Control 35:227–239CrossRefGoogle Scholar
  17. Jones VH (1945) The use of honey-dew as food by Indians. The Masterkey 19:145–149Google Scholar
  18. Kalinowski ST (2005) HP-RARE 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  19. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JL (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  20. Legner EF, Bellows TS (1999) Exploration for natural enemies. In: Fisher TW, Bellows TS (eds) Handbook of biological control. Academic Press, San Diego, CA, pp 87–101CrossRefGoogle Scholar
  21. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasion. Trends Ecol Evol 20:223–228PubMedCrossRefGoogle Scholar
  22. Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell, Malden, MAGoogle Scholar
  23. Loxdale HD, Lushai G (1999) Slaves of the environment: the movement of insects in relation to their ecology and genotype. Phil Trans R Soc Lond B 354:1479–1495CrossRefGoogle Scholar
  24. Lozier JD, Roderick GK, Mills NJ (2007) Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host pant associated species in the aphid genus Hyalopterus (Hemiptera: Aphididae) Evolution 61:1353–1367PubMedCrossRefGoogle Scholar
  25. Lozier JD, Miller GL, Foottit RG, Mills NJ, Roderick GK (2008) Molecular and morphological evaluation of the aphid genus Hyalopterus Koch (Insecta: Hemiptera: Aphididae), with a description of a new species. Zootaxa 1688:1–19Google Scholar
  26. Mack RN, Erneberg M (2002) The United States naturalized flora: largely the product of deliberate introductions. Ann Mo Bot Gard 89:176–189CrossRefGoogle Scholar
  27. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzazz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  28. Mills NJ (2000) Biological control: the need for realistic models and experimental approaches to parasitoid introductions. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, pp 217–234Google Scholar
  29. Minch E (1997) MICROSAT, Version 1.5b. Stanford University Medical Center, StanfordGoogle Scholar
  30. Nardi F, Carapelli A, Dallai R, Roderick GK, Frati F (2005) Population structure and colonization history of the olive fly, Bactrocera oleae (Diptera, Tephritidae). Mol Ecol 14:2729–2738PubMedCrossRefGoogle Scholar
  31. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  32. Nei M, Maruyma T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  33. Nieminen M, Leskin M, Helenius J (2000) Doppler radar detection of exceptional mass migration of aphids into Finland. Int J Biometeorol 44:172–181PubMedCrossRefGoogle Scholar
  34. Novak R, Mack RN (2001) Tracing plant introductions and spread in naturalized ranges: genetic evidence from Bromus tectorum (cheatgrass). BioScience 51:114–122CrossRefGoogle Scholar
  35. Pascual M, Chapuis MP, Mestres F, Balanyà 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
  36. Pastene LA, Goto M, Kanda N, Zerbini AN, Kerem D, Watanabe K, Bessho Y, Hasegawa M, Nielsen R, Larsen F, Palsbøll PJ (2007) Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata. Mol Ecol 16:1481–1495PubMedCrossRefGoogle Scholar
  37. Peterson MA, Denno RF (1998) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. Am Nat 152:428–446PubMedCrossRefGoogle Scholar
  38. 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 52:273–288CrossRefGoogle Scholar
  39. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: A software for genetic assignment and first generation migrants detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  40. Poulios KD, Margaritapoulos JT, Tsitsipis JA (2007) Morphological seperation of host adapted taxa within the Hyalopterus pruni complex (Hemiptera: Aphididae) Eur J Entomol 104:235–242Google Scholar
  41. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  42. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221PubMedCrossRefGoogle Scholar
  43. Raymond M, Rousset F (1995) GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  44. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  45. Roderick GK (2004) Tracing the origin of pests and natural enemies: genetic and statistical approaches. In: Ehler LE, Sforza R, Mateille T (eds) Genetics, Evolution, and Biological Control. CAB International, Wallingford, UK, pp 97–112Google Scholar
  46. Roderick GK, Navajas M (2003) Genes in new environments: genetics and evolution in biological control. Nature Rev Genet 4:889–899CrossRefGoogle Scholar
  47. Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc Lond B 273:2453–2459CrossRefGoogle Scholar
  48. Rosenberg NA, Mahajan S, Ramachandran S, Zhao C, Pritchard JK, Feldman MW (2006) Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genetics 1:e70. doi: 10.1371/journal.pgen.0010070
  49. Rousset F (1997) Genetic differentiation and estimations of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  50. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  51. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449PubMedCrossRefGoogle Scholar
  52. Saunders CF, Smeaton Chase J (1915) The California padres and their missions. Houghton-Mifflin, BostonGoogle Scholar
  53. Simberloff D, Von Holle B (1999) Positive interactions of nonindiginous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  54. Simon C, Franke A, Martin A (1991) The polymerase chain reaction: DNA extraction and amplification. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy. Springer-Verlag, Berlin, pp 329–355Google Scholar
  55. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701Google Scholar
  56. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  57. Smith LM (1936) Biology of the mealy plum aphid, Hyalopterus pruni (Geoffroy) Hilgardia 7:167–211Google Scholar
  58. Suarez AV, Tsutsui ND (2007) The evolutionary consequences of biological invasions. Mol Ecol (online early). doi: 10.1111/j.1365-294X.2007.03456.x
  59. Sunnucks P, De Barro PJ, Lushai G, Maclean N, Hales D (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Mol Ecol 6:1059–1073PubMedCrossRefGoogle Scholar
  60. Templeton AR (1998) Nested clade analysis of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397PubMedCrossRefGoogle Scholar
  61. Torbert E (1936) The specialized commercial agriculture of the northern Santa Clara valley. Geogr Rev 26:247–263CrossRefGoogle Scholar
  62. USDA (2006) 2006 California prune (dried plum) post-harvest estimate. National Agricultural Statistics Service Cited 29 Sept 2007
  63. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  64. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Jeffrey D. Lozier
    • 1
    • 2
  • George K. Roderick
    • 1
  • Nicholas J. Mills
    • 1
  1. 1.Department of Environmental SciencePolicy and Management, Mulford Hall, University of CaliforniaBerkeleyUSA
  2. 2.Department of EntomologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations