Advertisement

Evolutionary Ecology

, Volume 28, Issue 3, pp 505–520 | Cite as

Geographic variation in winter hardiness of a common agricultural pest, Leptinotarsa decemlineata, the Colorado potato beetle

  • Victor M. IzzoEmail author
  • David J. Hawthorne
  • Yolanda H. Chen
Original Paper

Abstract

Successful latitudinal expansions into temperate climates depend largely upon the evolution of novel adaptive traits or the presence of pre-adaptive or exapted mechanisms for survival in seasonal climates. Geographic comparisons of ancestral (pre-expansion) and derived (post-expansion) populations provide a useful framework for understanding the evolutionary conditions that facilitate geographic expansions. Using a common agricultural pest, the Colorado Potato Beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) as a model, we conducted a regional comparison of cold hardiness and overwintering success among ancestral (southern Mexico) and derived (Vermont and Kansas, USA) L. decemlineata populations. In order to determine if ancestral and derived beetle populations vary physiologically for cold hardiness, we compared supercooling points (SCPs) of three geographic populations of L. decemlineata. We also tested if ancestral and derived beetle populations differed in their overwintering behavior and success by performing an overwintering field experiment. Ancestral and derived populations did not express different physiological responses (i.e. SCPs) to freezing temperatures. However, ancestral and derived populations responded differently to the onset of winter conditions and displayed dissimilar overwintering behaviors. The majority of ancestral beetles failed to initiate diapause and dug upward within experimental mesocosms. Differences in overwintering behavior also resulted in significant variation in overwintering success as derived populations displayed higher overwintering survivorship when compared with ancestral populations. Given our results, it is evident that research exploring the interaction of the ecological factors and evolutionary processes is necessary to fully realize the dynamics of biological invasions.

Keywords

Evolutionary ecology Overwintering Behavior Invasions Diapause 

Notes

Acknowledgments

We would like to thank Jordan Armstrong for his technical assistance during the rearing of L. decemlineata populations and the University of Vermont Greenhouse Management Staff, especially Tom Doubleday, Dave Heleba and Colleen Armstrong for their experimental support. Furthermore, we would like to extend our gratitude to the late Scott Costa for the use of his supercooling equipment and support during the execution of the study. We are also grateful to Scott Lewins for his counsel during the length of the study and his review of the manuscript. We would also like to thank Liz Saccardi for her editorial comments. Finally we want to thank Charles Goodnight, Deborah Neher and Alison Brody of the University Vermont for their support and advisory roles during this project.

References

  1. Alyokhin A, Baker M, Mota-Sanchez D, Dively G, Grafius E (2008) Colorado potato beetle resistance to insecticides. Am J Potato Res 85:395–413CrossRefGoogle Scholar
  2. Baker MB, Alyokhin A, Porter AH, Ferro DN, Dastur SR, Galal N (2007) Persistence and inheritance of costs of resistance to imidacloprid in Colorado potato beetle. J Econ Entomol 100:1871–1879PubMedCrossRefGoogle Scholar
  3. Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc Lond B Biol Sci 357:849–862PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994PubMedCrossRefGoogle Scholar
  5. Boiteau G, Coleman W (1996) Cold tolerance in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Can Entomol 128:1087–1099CrossRefGoogle Scholar
  6. Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1–25CrossRefGoogle Scholar
  7. Cappaert DL (1988) Ecology of the Colorado potato beetle in Mexico. Michigan State University, East Lansing, MI, DissertatiGoogle Scholar
  8. Casagrande RA (1987) The Colorado potato beetle 125 years of mismanagement. Bull Entomol Soc Am 33:142–150Google Scholar
  9. Danks HV (2002) Modification of adverse conditions by insects. Oikos 99:10–24CrossRefGoogle Scholar
  10. Danks HV (2004) Seasonal adaptations in arctic insects. Integr Comp Biol 44:85–94PubMedCrossRefGoogle Scholar
  11. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93PubMedCrossRefGoogle Scholar
  12. Denlinger DL, Lee RE (2010) Low temperature biology of insects. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  13. Dhondt AA (1997) Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. J Anim Ecol 66:113CrossRefGoogle Scholar
  14. Diaz MDC, Peck DC (2007) Overwintering of annual bluegrass weevils, Listronotus maculicollis, in the golf course landscape. Entomol Exp Appl 125:259–268CrossRefGoogle Scholar
  15. Dingle H (2001) The evolution of migratory syndromes in insects. Insect Movement: Mechanisms and Consequences, p 159–181Google Scholar
  16. Duman JG, Wu DW, Xu L, Tursman D, Olsen TM (1991) Adaptations of insects to subzero temperatures. Q Rev Biol 66:387–410CrossRefGoogle Scholar
  17. Follett PA, Roderick GK (1996) Adaptation to insecticides in Colorado potato beetle: Single- and meta-population models. SPB Academic Publishing, Amersterdam, NetherlandsGoogle Scholar
  18. Gaston KJ (2003) The how and why of biodiversity. Nature 421:900–901PubMedCrossRefGoogle Scholar
  19. Gatehouse VAD and AG (1995) Insect Migration. Cambridge University Press: CambridgeGoogle Scholar
  20. Guillemaud T, Ciosi M, Lombaert E, Estoup A (2011) Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. CR Biol 334:237–246CrossRefGoogle Scholar
  21. Haack RA, Lawrence RK, Heaton GC (2001) Tomicus piniperda (Coleoptera: Scolytidae) shoot-feeding characteristics and overwintering behavior in scotch pine Christmas trees. J Econ Entomol 94:422–429PubMedCrossRefGoogle Scholar
  22. Hare JD (1990) Ecology and management of the Colorado potato beetle. Annu Rev Entomol 35:81–100CrossRefGoogle Scholar
  23. Hiiesaar K, Kuusik A, Joudu J, Metspalu L, Hermann P (2001) Laboratory experiments on cold acclimation in overwintering Colorado potato beetles, Leptinotarsa decemlineata (Say). Nor J Entomol 48:87–90Google Scholar
  24. Hiiesaar K, Metspalu L, Jõudu J, Jõgar K (2006) Over-wintering of the Colorado potato beetle (Leptinotarsa decemlineata Say) in field conditions and factors affecting its population density in Estonia. Agronomy Res 4:21–30Google Scholar
  25. Hochachka P, Somero G (2002) Biochemical adaptation: mechanism and process in physiological evolution, vol 480. Oxford University Press, New YorkGoogle Scholar
  26. Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–216CrossRefGoogle Scholar
  27. Hsiao TH (1981) Ecophysiological adaptations among geographic populations of the Colorado potato beetle in North America. in Advances in Potato Management, p 69–85Google Scholar
  28. Hsiao TH (1982) Inheritance of three autosomal mutations in the Colorado potato beetle, Leptinotarsa Decemlinieata (Coleoptera:Chrysomeldiae). Genome 24:681–686Google Scholar
  29. Hunt DWA, Tan CS (2000) Overwintering densities and survival of the Colorado potato beetle (Coleoptera: Chrysomelidae) in and around tomato (Solanaceae) fields. Can Entomol 132:103–105Google Scholar
  30. Jacobson J, Hsiao TH (1983) Isozyme variation between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 76:162–166Google Scholar
  31. Jacques RL (1988) The Potato Beetles: The Genus Leptinotarsa in North America (Coleoptera: Chrysomelidae). E. J, BrillGoogle Scholar
  32. Jepsen JU, Kapari L, Hagen SB, Schott T, Vindstad OPL, Nilssen AC, Ims RA (2011) Rapid northwards expansion of a forest insect pest attributed to spring phenology matching with sub-Arctic birch. Glob Change Biol 17:2071–2083. doi: 10.1111/j.1365-2486.2010.02370.x CrossRefGoogle Scholar
  33. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  34. Kellermann V, van Heerwaarden B, Sgrò CM, Hoffmann AA (2009) Fundamental evolutionary limits in ecological traits drive drosophila species distributions. Science 325:1244–1246PubMedCrossRefGoogle Scholar
  35. Kimura MT (1988) Adaptations to temperate climates and evolution of overwintering strategies in the drosophila melanogaster species group. Evolution 42:1288–1297CrossRefGoogle Scholar
  36. Koch RL, Carrillo MA, Venette RC, Cannon CA, Hutchison WD (2004) Cold hardiness of the multicolored asian lady beetle (Coleoptera: Coccinellidae). Environ Entomol 33:815–822CrossRefGoogle Scholar
  37. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  38. Kostál V, Simek P (1995) Dynamics of cold hardiness, supercooling and cryoprotectants in diapausing and non-diapausing pupae of the cabbage root fly, Delia radicum L. J Insect Physiol 41:627–634CrossRefGoogle Scholar
  39. Lee E (2002) Evolutionary genetics of invasive species. Trends in Ecol Evol 17:386–391CrossRefGoogle Scholar
  40. Lefevere K, Kort CAD (1989) Adult diapause in the Colorado potato beetle, Leptinotarsa decemlineata: effects of external factors on maintenance, termination and post-diapause development. Physiol Entomol 14:299–308CrossRefGoogle Scholar
  41. Lu W, Logan PA (1993) Induction of feeding on potato in Mexican Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Environ Entomol 22:759–765Google Scholar
  42. Lu WH, Logan P (1994) Inheritance of larval body color in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 87:454–459Google Scholar
  43. Lyytinen A, Lindstrom L, Mappes J (2008) Genetic variation in growth and development time under two selection regimes in Leptinotarsa decemlineata. Entomol Exp Appl 127:157–167CrossRefGoogle Scholar
  44. Lyytinen A, Boman S, Grapputo A, Lindström L, Mappes J (2009) Cold tolerance during larval development: effects on the thermal distribution limits of Leptinotarsa decemlineata. Entomol Exp Appl 133:92–99CrossRefGoogle Scholar
  45. Nault BA, Hanzlik MW, Kennedy GG (1997) Location and abundance of adult Colorado potato beetles (Coleoptera: Chrysomelidae) following potato harvest. Crop Prot 16:511–518Google Scholar
  46. Nelson RJ, Denlinger DL, Somers DE (2010) Photoperiodism: The Biological Calendar. Oxford University Press, OxfordGoogle Scholar
  47. Piiroinen S, Ketola T, Lyytinen A, Lindström L (2011) Energy use, diapause behaviour and northern range expansion potential in the invasive Colorado potato beetle. Funct Ecol 25:527–536CrossRefGoogle Scholar
  48. Rako L, Hoffmann AA (2006) Complexity of the cold acclimation response in Drosophila melanogaster. J Insect Physiol 52:94–104PubMedCrossRefGoogle Scholar
  49. Renault D, Salin C, Vannier G, Vernon P (2002) Survival at low temperatures in insects: what is the ecological significance of the supercooling point? Cryo Letters 23:217–228PubMedGoogle Scholar
  50. Salt RW (1961) Principles of insect cold-hardiness. Annu Rev Entomol 6:55–74CrossRefGoogle Scholar
  51. Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2010) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436CrossRefGoogle Scholar
  52. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  53. Sinclair BJ, Addo-Bediako A, Chown SL (2003a) Climatic variability and the evolution of insect freeze tolerance. Biol Rev Camb Philos Soc 78:181–195PubMedCrossRefGoogle Scholar
  54. Sinclair BJ, Vernon P, Jaco Klok C, Chown SL (2003b) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262CrossRefGoogle Scholar
  55. Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A Physiol 73:519–543CrossRefGoogle Scholar
  56. Stastny M, Battisti A, Petrucco-Toffolo E, Schlyter F, Larsson S (2006) Host-plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa. Ecol Entomol 31:481–490. doi: 10.1111/j.1365-2311.2006.00807.x CrossRefGoogle Scholar
  57. Tauber MJ, Tauber CA, Obrycki JJ, Gollands B, Wright RJ (1988) Geographical variation in responses to photoperiod and temperature by Leptinotarsa Decemlineata (Coleoptera, Chrysomelidae) during and after dormancy. Ann Entomol Soc Am 81:764–773Google Scholar
  58. Tower W (1906) Investigation of evolution in chrysomelid beetles of the genus Leptinotarsa. Carnegie Institution of Washington, WashingtonGoogle Scholar
  59. Turnock WIJ, Fields P (2005) Winter climates and coldhardiness in terrestrial insects, p 561–576Google Scholar
  60. Weber D (2003) Colorado beetle: pest on the move. Pestic Outlook 14:256CrossRefGoogle Scholar
  61. Weber DC, Ferro DN (1993) Distribution of overwintering Colorado potato beetle in and near massachusetts potato fields. Entomol Exp Appl 66:191–196Google Scholar
  62. Zachariassen KE, Kristiansen E, Pedersen SA, Hammel HT (2004) Ice nucleation in solutions and freeze-avoiding insects-homogeneous or heterogeneous? Cryobiology 48:309–321PubMedCrossRefGoogle Scholar
  63. Zehnder GW, Sandall L, Tisler AM, Powers TO (1992) Mitochondrial-DNA diversity among 17 geographic populations of Leptinotarsa Decemlineata (Coleoptera Chrysomelidae). Ann Entomol Soc Am 85:234–240Google Scholar
  64. Zhou Z-S, Guo J-Y, Michaud JP, Li M, Wan F-H (2011) Variation in cold hardiness among geographic populations of the ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), a biological control agent of Ambrosia artemisiifolia L. (Asterales: Asteraceae), in China. Biol Invasions 13:659–667CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Victor M. Izzo
    • 1
    Email author
  • David J. Hawthorne
    • 2
  • Yolanda H. Chen
    • 1
  1. 1.Plant and Soil Science DepartmentUniversity of VermontBurlingtonUSA
  2. 2.Department of EntomologyUniversity of MarylandCollege ParkUSA

Personalised recommendations