Skip to main content
Log in

Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States

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

Abstract

Introduced organisms experience founder effects including genetic bottlenecks that result in significant reductions in genetic variation. Genetic bottlenecks may constrain the evolution of phenotypic traits that facilitate success in novel habitats. We examined the effect of introduction into novel environments on genetic diversity of an insect pest, Adelges cooleyi, which was introduced into the eastern United States during the mid nineteenth century. We compared variation in mitochondrial and nuclear genomes in native and introduced samples to determine the effect of introduction on genetic variation experienced by this insect. We also measured an ecologically important phenotype, variation in host preference, in both native and introduced samples to compare variation in that trait with molecular genetic variation. To further investigate the relationship between genetic and phenotypic variation, we examined the degree to which mtDNA haplotypes provide information about host preference. Adelges cooleyi in eastern North America has significantly reduced genetic and phenotypic variation, but this low variation does not appear to have prevented persistence in a novel environment. Introduced insects appear to have retained host preference phenotypes similar to those of insects found where introductions likely originated.

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

Similar content being viewed by others

References

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326. doi:10.1126/science.1060701

    Article  PubMed  CAS  Google Scholar 

  • Ahern RG, Hawthorne DJ, Raupp MJ (2008) Phylogeography of a specialist insect, Adelges cooleyi: historical and contemporary processes shape the distribution of population genetic variation. Mol Ecol (submitted)

  • Annand PN (1928) A contribution toward a monograph of the Adelginae (Phylloxeridae) of North America. Biol Sci 6:2–146

    Google Scholar 

  • Apple ME, Olszyk DM, Ormrod DP et al (2000) Morphology and stomatal function of Douglas fir needles exposed to climate change: elevated CO2 and temperature. Int J Plant Sci 161:127–132. doi:10.1086/314237

    Article  PubMed  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Drake JA (eds) The genetics of colonizing species. Academic Press, New York, pp 147–172

    Google Scholar 

  • Brennan EB, Weinbaum SA (2001) Effect of epicuticular wax on adhesion of psyllids to glaucous juvenile and glossy adult leaves of Eucalyptus globulus Labillardiere. Aust J Entomol 40:270–277. doi:10.1046/j.1440-6055.2001.00229.x

    Article  Google Scholar 

  • Burdon JJ, Thrall PH (2004) Genetic structure of natural plant and pathogen populations. In: Ehler LE, Sforza R, Mateille T (eds) Genetics, evolution and biological control. CABI Publishing, Cambridge, pp 1–15

    Google Scholar 

  • Cock MJW (1978) The assessment of preference. J Anim Ecol 47:805–816. doi:10.2307/3672

    Article  Google Scholar 

  • Cox GW (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes and interacting native species. Island Press, Washington

    Google Scholar 

  • Cranshaw WS (1989) Patterns of gall formation by the Cooley spruce gall adelgid on Colorado blue spruce. J Arboric 15:277–288

    Google Scholar 

  • Dlugosch KM, Parker IM (2007) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  PubMed  Google Scholar 

  • Drake JM (2004) Allee effects and the risk of biological invasion. Risk Anal 24:795–802. doi:10.1111/j.0272-4332.2004.00479.x

    Article  PubMed  Google Scholar 

  • Drake JM, Lodge DM (2006) Allee effects, propagule pressue and the probability of establishment: risk analysis for biological invasions. Biol Invasions 8:365–375. doi:10.1007/s10530-004-8122-6

    Article  Google Scholar 

  • Eigenbrode SD (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194. doi:10.1146/annurev.en.40.010195.001131

    Article  Google Scholar 

  • Elderkin CL, Perkins EJ, Leberg PL, Klerks PL, Lance RF (2004) Amplified fragment length polymorphism (AFLP) analysis of the genetic structure of the zebra mussel, Dreissena polymorpha, in the Mississippi River. Freshw Biol 49:1487–1494. doi:10.1111/j.1365-2427.2004.01285.x

    Article  CAS  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050. doi:10.1073/pnas.97.13.7043

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Feder JL, Chilcote CA, Bush GL (1990) The geographic patterns of genetic differentiation between host associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evol Int J Org Evol 44:570–594. doi:10.2307/2409436

    Google Scholar 

  • Futuyma DJ, McCafferty (1990) Phylogeny and the evolution of host plant associations in the leaf beetle Ophraella (Coleopter, Chrysomelidae). Evol Int J Org Evol 44:1885–1913. doi:10.2307/2409602

    Google Scholar 

  • Futuyma DJ, Peterson SC (1985) Genetic variation in the use of resources by insects. Annu Rev Entomol 30:217–238. doi:10.1146/annurev.en.30.010185.001245

    Article  Google Scholar 

  • Gillette CP (1907) Chermes of Colorado conifers. Proc Natl Acad Sci Philadelphia 59:3–22

    Google Scholar 

  • Grapputo A, Boman S, Lindstrom L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219

    PubMed  CAS  Google Scholar 

  • Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci USA 103:968–971. doi:10.1073/pnas.0510466103

    Article  PubMed  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Hastings A, Cuddington K, Davies KF et al (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 1:91–101. doi:10.1111/j.1461-0248.2004.00687.x

    Article  Google Scholar 

  • Hawthorne DJ (1997) Ecological hostory and evolution in a novel environment: habitat heterogeneity and insect adaptation to a new host plant. Evol Int J Org Evol 51:153–162. doi:10.2307/2410968

    Google Scholar 

  • Hedrick PW, Ginevan ME, Ewing EP (1976) Genetic polymorphism in heterogeneous environments. Annu Rev Ecol Syst 7:1–32. doi:10.1146/annurev.es.07.110176.000245

    Article  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Google Scholar 

  • Hewitt GM (2001) Speciation, hybrid zones, and phylogeography – or seeing genes in space and time. Mol Ecol 10:537–549. doi:10.1046/j.1365-294x.2001.01202.x

    Article  PubMed  CAS  Google Scholar 

  • Iline II, Phillips CB (2004) Allozyme markers to help define the South American origins of Microctonus hyperodae (Hymenoptera: Braconidae) established in New Zealand for biological control of Argentine stem weevil. Bull Entomol Res 94:229–234. doi:10.1079/BER2004303

    Article  PubMed  CAS  Google Scholar 

  • Ivanova NV, de Waard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002. doi:10.1111/j.1471-8286.2006.01428.x

    Article  CAS  Google Scholar 

  • Johnston JA, Donovan LA, Arnold ML (2004) Novel phenotypes among early generation hybrids of two Louisiana iris species: flooding experiments. J Ecol 92:967–976. doi:10.1111/j.1365-2745.2004.00939.x

    Article  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR et al (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181. doi:10.1038/nature02807

    Article  PubMed  CAS  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. doi:10.1016/S0169-5347(02)02554-5

    Article  Google Scholar 

  • Leung B, Drake JM, Lodge DM (2004) Predicting invasions: propagule pressure and the gravity of allee effect. Ecology 85:1651–1660. doi:10.1890/02-0571

    Article  Google Scholar 

  • Li P, Adams WT (1989) Range-wide patterns of allozyme variation in Douglas-fir (Pseudotsuga menziesii). Can J For Res 19:149–161. doi:10.1139/x89-022

    Article  Google Scholar 

  • Lipscomb B (1993) Flora of North America North of Mexico. Oxford Univerity Press, New York and Oxford

    Google Scholar 

  • Little EL Jr (1971) Atlas of the United States trees, volume 1, conifers and important hardwoods, pp. 9, 200 maps. U.S. Department of Agriculture

  • Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. doi:10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2

    Article  Google Scholar 

  • Mackauer M (1976) Genetic problems in the production of biological control agents. Annu Rev Entomol 21:369–385. doi:10.1146/annurev.en.21.010176.002101

    Article  Google Scholar 

  • Mock KE, Bentz BJ, O’Neill EM et al (2007) Landscape-scale genetic variation in a forest outbreak species, the mountain pine beetle (Dendroctonus ponderosae). Mol Ecol 16:553–568. doi:10.1111/j.1365-294X.2006.03158.x

    Article  PubMed  CAS  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451. doi:10.1073/pnas.091093398

    Article  PubMed  CAS  Google Scholar 

  • Moran NA (1988) The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. Am Nat 132:681–706. doi:10.1086/284882

    Article  Google Scholar 

  • Muluvi GM, Sprent JI, Soranzo N et al (1999) Amplified fragment length polymorphism (AFLP) analysis of genetic variation in Moringa oleifera Lam. Mol Ecol 8:463–470. doi:10.1046/j.1365-294X.1999.00589.x

    Article  PubMed  CAS  Google Scholar 

  • Parsons YM, Shaw KL (2001) Species boundaries and genetic diversity among Hawaiian crickets from the genus Laupala identified using amplified fragment length polymorphism. Mol Ecol 10:1765–1772. doi:10.1046/j.1365-294X.2001.01318.x

    Article  PubMed  CAS  Google Scholar 

  • Price PW (1997) Insect ecology, 3rd edn. John Wiley & Sons, Inc., New York

    Google Scholar 

  • Rehfeldt GE (1977) Growth and cold hardiness of intervarietal hybrids of Douglas-fir. Theor Appl Genet 50:3–15. doi:10.1007/BF00273790

    Article  Google Scholar 

  • Rehfeldt GE (1978) The genetic structure of a population of Douglas-fir (Pseudotruga menziesii var. glauca) as reflected by its wind-pollinated progenies. Silvae Genet 27:49–52

    Google Scholar 

  • Reveal J (1992) Gentle conquest: the botanical discovery of North America with illustrations from the Library of Congress. Starwood Publishing, Washington

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109. doi:10.1146/annurev.ecolsys.27.1.83

    Article  Google Scholar 

  • Scheffer SJ, Grissell EE (2003) Tracing the geographical origin of Megastigmus transvaalensis (Hymenoptera: Torymidae): an African wasp feeding on a South American plant in North America. Mol Ecol 12:415–421. doi:10.1046/j.1365-294X.2003.01725.x

    Article  PubMed  Google Scholar 

  • Stadler T, Frye M, Neiman M, Lively CM (2005) Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail. Mol Ecol 14:2465–2473. doi:10.1111/j.1365-294X.2005.02603.x

    Article  PubMed  CAS  Google Scholar 

  • Stephan BR (1987) Differences in the resistance if Douglas fir provenances to the woolly aphid Gilletteella cooleyi. Silvae Genet 36:76–79

    Google Scholar 

  • Suarez AV, Tsutsui ND, Holway DA, Case TJ (2004) Behavioral and genetic differentiation between native and introduced population of the Argentine ant. Biol Invasions 1:43–53. doi:10.1023/A:1010038413690

    Article  Google Scholar 

  • Sullivan JH, Teramura AH (1988) Effects of ultra-violet-B irradiation on seed growth in the Pinaceae. Am J Bot 75:225–230. doi:10.2307/2443888

    Article  Google Scholar 

  • Taylor AC, Cowan PE, Fricke BL et al (2004) High microsatellite diversity and differential structuring among populations of the introduced common brushtail possum, Trichosurus vulpecula, in New Zealand. Genet Res 83:101–111. doi:10.1017/S001667230400672X

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953. doi:10.1073/pnas.100110397

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2001) Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and the source of introduced populations. Mol Ecol 10:2151–2161. doi:10.1046/j.0962-1083.2001.01363.x

    Article  PubMed  CAS  Google Scholar 

  • Via S (1991) The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evol Int J Org Evol 45:827–852. doi:10.2307/2409692

    Google Scholar 

  • Vos P, Hogers R, Bleeker M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414. doi:10.1093/nar/23.21.4407

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1998) Biostatistical analysis, 4th edn. Prentice Hall, Upper Sadle River

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank Galen Dively, Matthew Hare, Sonja Scheffer, Kerry Shaw, and four anonymous reviewers for valuable comments that improved an earlier version of this manuscript. Bob Foottit and Nathan Havill provided expertise and primers, respectively. Joan West provided technical assistance, and Whitney Cranshaw, Ruth Hufbauer, Carol von Dohlen, and Jill O’Donnell assisted with collection and collection trips. We would also like to thank Susan Newhart, Larry May, Don and Joan Hilliker; David Walker; Tom Brobson and David Brady for graciously allowing and facilitating collection efforts on their personal property. Sequencing was supported by funding to the Canadian Barcode of Life Network from Genome Canada (through the Ontario Genomics Institute), NSERC and other sponsors listed at www.BOLNET.ca.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert G. Ahern.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahern, R.G., Hawthorne, D.J. & Raupp, M.J. Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States. Biol Invasions 11, 959–971 (2009). https://doi.org/10.1007/s10530-008-9308-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-008-9308-0

Keywords

Navigation