Stress for invasion success? Temperature stress of preceding generations modifies the response to insecticide stress in an invasive pest insect

Evolutionary Applications

Volumn 6, Issue 2, 2013, Pages 313-323

  Piiroinen, Saija ^a   Lyytinen, Anne ^a   Lindström, Leena ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

Adaptive phenotypic plasticity; Carry over; Cross generational effect; Invasive species; Pyrethroids; Species range; Stress tolerance; Sub lethal effects

Indexed keywords

EID: 84874090574     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12001     Document Type: Article

References (80)

1. Addo-Bediako, A., S. L. Chown, and K. J. Gaston 2000. Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London. Series B, Biological Sciences 267:739-745.
2. Alyokhin, A., M. Baker, D. Mota-Sanchez, G. Dively, and E. Grafius 2008. Colorado potato beetle resistance to insecticides. American Journal of Potato Research 85:395-413.
3. Angers, B., E. Castonguay, and R. Massicotte 2010. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Molecular Ecology 19:1283-1295.
4. Argentine, J. A., S. H. Lee, M. A. Sos, S. R. Barry, and J. M. Clark 1995. Permethrin resistance in a near isogenic strain of Colorado potato beetle. Pesticide Biochemistry and Physiology 53:97-115.
5. Badyaev, A. V. 2005. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proceedings of the Royal Society of London. Series B, Biological Sciences 272:877-886.
6. Bates, D. M., M. Maechler, and B. Bolker 2011. lme4:Linear mixed-effects models using S4 classes. R package version 0.999375-39.
7. Bernard, L., and L. Lagadic 1993. Sublethal effects of dietary cyfluthrin on nutritional performance and gut hydrolase activity in larvae of the Egyptian cotton leafworm, Spodoptera littoralis. Pesticide Biochemistry and Physiology 46:171-180.
8. Boman, S., A. Grapputo, L. Lindström, A. Lyytinen, and J. Mappes 2008. Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits. Biological Invasions 10:1135-1145.
9. Bonduriansky, R., and T. Day 2009. Nongenetic inheritance and evolutionary implications. Annual Review of Ecology, Evolution and Systematics 40:103-125.
10. Bossdorf, O., C. L. Richards, and M. Pigliucci 2008. Epigenetics for ecologists. Ecology Letters 11:106-115.
11. Campero, M., S. Slos, F. Ollevier, and R. Stoks 2007. Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms. Ecological Applications 17:2111-2122.
12. Casagrande, R. A. 1987. The Colorado potato beetle: 125 years of mismanagement. Bulletin of the Entomological Society of America 33:142-150.
13. Castaneda, L., M. Lardies, and F. Bozinovic 2004. Adaptive latitudinal shifts in the thermal physiology of a terrestrial isopod. Evolutionary Ecology Research 6:579-593.
14. Cohen, E. 2006. Pesticide-mediated homeostatic modulation in arthropods. Pesticide Biochemistry and Physiology 85:21-27.
15. ffrench-Constant, R. H., P. J. Daborn, and G. L. Goff 2004. The genetics and genomics of insecticide resistance. Trends in Genetics 20:163-170.
16. Coors, A., and L. De Meester 2008. Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna. Journal of Applied Ecology 45:1820-1828.
17. Costantini, D., N. B. Metcalfe, and P. Monaghan 2010. Ecological processes in a hormetic framework. Ecology Letters 13:1435-1447.
18. Crill, W. D., R. B. Huey, and G. W. Gilchrist 1996. Within- and between-generation effects of temperature on the morphology and physiology of Drosophila melanogaster. Evolution 50:1205-1218.
19. Cutler, G. C., C. D. Scott-Dupree, J. H. Tolman, and C. R. Harris 2005. Acute and sublethal toxicity of novaluron, a novel chitin synthesis inhibitor, to Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Pest Management Science 61:1060-1068.
20. Desneux, N., A. Decourtye, and J. M. Delpuech 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52:81-106.
21. Duckworth, R. A. 2009. Maternal effects and range expansion: a key factor in a dynamic process? Philosophical Transactions of the Royal Society of London, Series B, Biological sciences 364:1075-1086.
22. Dyer, A. R., C. S. Brown, E. K. Espeland, J. K. McKay, H. Meimberg, and K. J. Rice 2010. The role of adaptive trans-generational plasticity in biological invasions of plants. Evolutionary Applications 3:179-192.
23. Easterling, D., G. Meehl, C. Parmesan, S. Changnon, T. Karl, and L. Mearns 2000. Climate extremes: observations, modeling, and impacts. Science 289:2068-2074.
24. EPPO. 2006. Distribution Maps of Quarantine Pests for Europe, Leptinotarsa decemlineata. ADAS, Nottingham, UK.
25. Fagerström, T., and C. Wiklund 1982. Why do males emerge before females - protandry as a mating strategy in male and female butterflies. Oecologia 52:164-166.
26. Ferro, D. N., J. A. Logan, R. H. Voss, and J. S. Elkinton 1985. Colorado potato beetle (Coleoptera: Chrysomelidae) temperature-dependent growth and feeding rates. Environmental Entomology 14:343-348.
27. Fischer, K., and K. Fiedler 2000. Sex-related differences in reaction norms in the butterfly Lycaena tityrus (Lepidoptera: Lycaenidae). Oikos 90:372-380.
28. Gilchrist, G. W., L. M. Jeffers, B. West, D. G. Folk, J. Suess, and R. B. Huey 2008. Clinal patterns of desiccation and starvation resistance in ancestral and invading populations of Drosophila subobscura. Evolutionary Applications 1:513-523.
29. Grapputo, A., S. Boman, L. Lindström, A. Lyytinen, and J. Mappes 2005. The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Molecular Ecology 14:4207-4219.
30. Hahn, D. A., and D. L. Denlinger 2007. Meeting the energetic demands of insect diapause: nutrient storage and utilization. Journal of Insect Physiology 53:760-773.
31. Hardin, M. R., B. Benrey, M. Coll, W. O. Lamp, G. K. Roderick, and P. Barbosa 1995. Arthropod pest resurgence: an overview of potential mechanisms. Crop Protection 14:3-18.
32. Hoffmann, A. A., and M. J. Hercus 2000. Environmental stress as an evolutionary force. BioScience 50:217-226.
33. Hoffmann, A. A., and P. A. Parsons 1989. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics 122:837-845.
34. Hufbauer, R. A., B. Facon, V. Ravigne, J. Turgeon, J. Foucaud, C. E. Lee, O. Rey et al. 2012. Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evolutionary Applications 5:89-101.
35. Karl, I., K. H. Hoffmann, and K. Fischer 2010. Food stress sensitivity and flight performance across phosphoglucose isomerase enzyme genotypes in the sooty copper butterfly. Population Ecology 52:307-315.
36. Kellermann, V., B. Van Heerwaarden, C. M. Sgro, and A. A. Hoffmann 2009. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325:1244-1246.
37. Kolar, C. S., and D. M. Lodge 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16:199-204.
38. Lardies, M. A., T. P. Catalan, and F. Bozinovic 2004. Metabolism and life-history correlates in a lowland and highland population of a terrestrial isopod. Canadian Journal of Zoology 82:677-687.
39. Lee, C. E. 2002. Evolutionary genetics of invasive species. Trends in Ecology & Evolution 17:386-391.
40. Lee, C. E., and G. W. Gelembiuk 2008. Evolutionary origins of invasive populations. Evolutionary Applications 1:427-448.
41. Lee, C. E., J. L. Remfert, and G. W. Gelembiuk 2003. Evolution of physiological tolerance and performance during freshwater invasions. Integrative and Comparative Biology 43:439-449.
42. Lee, J. E., C. Janion, E. Marais, B. J. Van Vuuren, and S. L. Chown 2009. Physiological tolerances account for range limits and abundance structure in an invasive slug. Proceedings of the Royal Society of London. Series B, Biological Sciences 276:1459-1468.
43. Lehmann, P., A. Lyytinen, T. Sinisalo, and L. Lindström 2012. Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata). Journal of Insect Physiology, 58:1146-1158.
44. Lockwood, J. L., M. F. Hoopes, and M. P. Marchetti 2007. Invasion Ecology. Blackwell Publishing, Oxford, UK.
45. Lyytinen, A., S. Boman, A. Grapputo, L. Lindström, and J. Mappes 2009. Cold tolerance during larval development: effects on the thermal distribution limits of Leptinotarsa decemlineata. Entomologia Experimentalis et Applicata 133:92-99.
46. Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10:689-710.
47. Magiafoglou, A., and A. A. Hoffmann 2003. Cross-generation effects due to cold exposure in Drosophila serrata. Functional Ecology 17:664-672.
48. Maltby, L. 1999. Studying stress: the importance of organism-level responses. Ecological Applications 9:431-440.
49. McKenzie, J. A. 2001. Pesticide resistance. In C. A. Fox, D. A. Rolf, and D. J. Fairbairn, eds. Evolutionary Ecology; Concepts and Case Studies, pp. 347-360. Oxford University Press, New York.
50. Memmott, J., P. G. Craze, H. M. Harman, P. Syrett, and S. V. Fowler 2005. The effect of propagule size on the invasion of an alien insect. Journal of Animal Ecology 74:50-62.
51. Morse, J. G. 1998. Agricultural implications of pesticide-induced hormesis of insects and mites. Human & Experimental toxicology 17:266-269.
52. Mousseau, T. A., and C. W. Fox 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13:403-407.
53. Östman, Ö. 2005. Asynchronous temporal variation among sites in condition of two carabid species. Ecological Entomology 30:63-69.
54. Parsons, P. A. 1991. Evolutionary rates: stress and species boundaries. Annual Review of Ecology and Systematics 22:1-18.
55. Partridge, L., B. Barrie, N. H. Barton, K. Fowler, and V. French 1995. Rapid laboratory evolution of adult life-history traits in Drosophila melanogaster in response to temperature. Evolution 49:538-544.
56. Piiroinen, S. 2010. Range expansion to novel environments: evolutionary physiology and genetics in Leptinotarsa decemlineata. Jyväskylä Studies in Biological and Environmental Science, 155p.
57. Piiroinen, S., L. Lindström, and A. Lyytinen 2010. Resting metabolic rate can vary with age independently from body mass changes in the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Insect Physiology 56:277-282.
58. Piiroinen, S., T. Ketola, A. Lyytinen, and L. Lindström 2011. Energy use, diapause behaviour and northern range expansion potential in the invasive Colorado potato beetle. Functional Ecology 25:527-536.
59. Pimentel, D., L. Lach, R. Zuniga, and D. Morrison 2000. Environmental and economic costs of nonindigenous species in the United States. BioScience 50:53-64.
60. Puth, L., and D. Post 2005. Studying invasion: have we missed the boat? Ecology Letters 8:715-721.
61. Quinlan, R. J., and A. G. Gatehouse 1981. The effect of low doses of endosulfan on lipid reserves of the tsetse fly Glossina morsitans morsitans. Entomologia Experimentalis et Applicata 29:29-38.
62. R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R foundation for Statistical Computing, Vienna, Austria.
63. Richards, C. L., O. Bossdorf, N. Z. Muth, J. Gurevitch, and M. Pigliucci 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9:981-993.
64. Roderick, G. K., and M. Navajas 2003. Genes in new environments: genetics and evolution in biological control. Nature Reviews Genetics 4:889-899.
65. Roff, D. A. 2002. Life History Evolution. Sinauer Associates, Sunderland, MA, USA.
66. Sexton, J. P., J. K. Mckay, and A. Sala 2002. Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecological Applications 12:1652-1660.
67. Sih, A., A. M. Bell, and J. L. Kerby 2004. Two stressors are far deadlier than one. Trends in Ecology & Evolution 19:274-276.
68. Sokal, R. R., and F. J. Rohlf 2003. Biometry, The Principles and Practice of Statistics in Biological Research. W.H. Freeman and Company, New York, USA.
69. Steigenga, M. J., and K. Fischer 2007. Within- and between-generation effects of temperature on life-history traits in a butterfly. Journal of Thermal Biology 32:396-405.
70. Stoks, R., M. De Block, S. Slos, W. Van Doorslaer, and J. Rolff 2006. Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology 87:809-815.
71. Talloen, W., S. Van Dongen, H. Van Dyck, and L. Lens 2009. Environmental stress and quantitative genetic variation in butterfly wing characteristics. Evolutionary Ecology 23:473-485.
72. Tan, K. H. 1981. Antifeeding effect of cypermethrin and permethrin at sub-lethal levels against Pieris brassicae larvae. Pesticide Science 12:619-626.
73. Thrall, P. H., J. G. Oakeshott, G. Fitt, S. Southerton, J. J. Burdon, A. Sheppard, R. J. Russell et al. 2011. Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evolutionary Applications 4:200-215.
74. Tseng, M. 2004. Sex-specific response of a mosquito to parasites and crowding. Proceedings of the Royal Society of London. Series B, Biological Sciences 271:S186-S188.
75. Wang, D., P. Gong, M. Li, X. Qiu, and K. Wang 2009. Sublethal effects of spinosad on survival, growth and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae). Pest Management Science 65:223-227.
76. Wegorek, P., M. Pawinska, E. Przybysz, and R. Dutton 2002. Insecticide resistance management strategy for Colorado potato beetle (Leptinotarsa decemlineata Say) in Poland. Resistance Pest Management Newsletter 11:22-30.
77. Weir, S. M., and C. J. Salice 2012. High tolerance to abiotic stressors and invasion success of the slow growing freshwater snail, Melanoides tuberculatus. Biological Invasions 14:385-394.
78. Whalon, M. E., D. Mota-Sanchez, and R. M. Hollingworth, eds 2008. Global Pesticide Resistance in Arthropods. CAB International, Oxfordshire, UK.
79. Willi, Y., J. van Buskirk, B. Schmid, and M. Fischer 2006. Genetic isolation of fragmented populations is exacerbated by drift and selection. Journal of Evolutionary Biology 20:534-542.
80. Yin, X., Q. Wu, X. Li, Y. Zhang, and B. Xu 2009. Demographic changes in multigeneration Plutella xylostella (Lepidoptera: Plutellidae) after exposure to sublethal concentrations of spinosad. Journal of Economic Entomology 102:357-365.