Transgenerational effects of herbivory in a group of long-lived tree species: Maternal damage reduces offspring allocation to resistance traits, but not growth

Journal of Ecology

Volumn 101, Issue 4, 2013, Pages 1062-1073

  Holeski, Liza M ^a   Zinkgraf, Matthew S ^b   Couture, John J ^a   Whitham, Thomas G ^b   Lindroth, Richard L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

Cottonwood; Herbivory; Plant herbivore interactions; Plasticity; Populus; Resistance; Transgenerational

Indexed keywords

BEETLE; DECIDUOUS TREE; EVOLUTIONARY BIOLOGY; GROWTH RATE; HERBIVORY; HYBRID; LARVA; LIFE HISTORY TRAIT; MATERNAL EFFECT; PHENOTYPIC PLASTICITY; PHYTOCHEMISTRY; PLANT-HERBIVORE INTERACTION; RESOURCE ALLOCATION; SEEDLING;

ANIMALIA; CHRYSOMELA SCRIPTA; CHRYSOMELIDAE; POPULUS; POPULUS ANGUSTIFOLIA; POPULUS FREMONTII;

EID: 84879607383     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12110     Document Type: Article

References (96)

1. Agrawal, A.A. (2001) Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? American Naturalist, 157, 555-569.
2. Agrawal, A.A. (2002) Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance. Ecology, 83, 3408-3415.
3. Agrawal, A.A. & Karban, R. (1999) Why induced defenses may be favored over constitutive defenses in plants. The Ecology and Evolution of Inducible Defenses (eds R. Tollrian & C.D. Harvell ), pp. 45-61. Princeton University Press, Princeton, NY.
4. Agrawal, A.A., Laforsch, C. & Tollrian, R. (1999) Transgenerational induction of defenses in plants and animals. Nature, 401, 60-63.
5. Anderson, E.C. & Thompson, E.A. (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229.
6. Arnold, M.L. & Hodges, S.A. (1995) Are natural hybrids fit or unfit relative to their parents? Trends in Ecology and Evolution, 10, 67-71.
7. Ayres, M.P., Clausen, T.P., MacLean, S.F. Jr, Redman, A.M. & Reichardt, P.B. (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology, 78, 1696-1712.
8. Baldwin, I.T. & Karb, M.J. (1995) Plasticity in allocation of nicotine to reproductive parts in Nicotiana attenuata. Journal of Chemical Ecology, 21, 897-909.
9. Bangert, R.K., Allan, G.J., Turek, R.J., Wimp, G.M., Meneses, N., Martinsen, G.D., Keim, P. & Whitham, T.G. (2006) A genetic similarity rule determines arthropod community structure. Molecular Ecology, 15, 1379-1392.
10. Barton, K.E. & Koricheva, J. (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. American Naturalist, 175, 481-493.
11. Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution, 20, 441-448.
12. Bonduriansky, R. & Day, T. (2009) Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology, Evolution, and Systematics, 40, 103-125.
13. Braatne, J.H., Rood, S. & Heilman, P.E. (1996) Life history, ecology, and conservation of riparian cottonwoods in North America. Biology of Populus and its Implications for Management and Conservation (ed. R.F. Steller ), pp. 57-85. National Research Council of Canada, NRC Research Press, Ottawa, ON.
14. Cipollini, D., Purrington, C.B. & Bergelson, J. (2003) Costs of induced responses in plants. Basic and Applied Ecology, 4, 79-89.
15. Couture, J.J. (2011) Impacts of elevated carbon dioxide and ozone on community herbivory in a northern temperate forest. PhD Thesis, University of Wisconsin, Madison.
16. Dickson, T.L. & Mitchell, C.E. (2010) Herbivore and fungal pathogen exclusion affects the seed production of four common grassland species. PLoS ONE, 5, e12022.
17. Donaldson, J.R. & Lindroth, R.L. (2004) Cottonwood leaf beetle (Coleoptera: Chrysomelidae) performance in relation to variable phytochemistry in juvenile aspen (Populus tremuloides Michx.). Environmental Entomology, 33, 1505-1511.
18. Donaldson, J.R., Stevens, M.T., Barnhill, H.R. & Lindroth, R.L. (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). Journal of Chemical Ecology, 32, 1415-1429.
19. Elger, A., Lemoine, D.G., Fenner, M. & Hanley, M.E. (2009) Plant ontogeny and chemical defence: older seedlings are better defended. Oikos, 118, 767-773.
20. Floate, K.D., Kearsley, M.J.C. & Whitham, T.G. (1993) Elevated herbivory in plant hybrid zones- Chrysomela confluens, Populus, and phonological sinks. Ecology, 74, 2056-2065.
21. Floate, K.D. & Whitham, T.G. (1994) Ant-aphid interaction reduces Chrysomelid herbivory in a cottonwood hybrid zone. Oecologia, 97, 215-221.
22. Fritz, R.S., Hochwender, C.G., Lewkiewicz, D.A., Bothwell, S. & Orians, C.M. (2001) Seedling herbivory by slugs in a willow hybrid system: developmental changes in damage, chemical defense, and plant performance. Oecologia, 129, 87-97.
23. Galloway, L.F. (1995) Response to natural environmental heterogeneity: maternal effects and selection on life-history characters and plasticities in Mimulus guttatus. Evolution, 49, 1095-1107.
24. 2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda). Oecologia, 113, 29-36.
25. Goodger, J.Q.D., Choo, T.Y.S. & Woodrow, I.E. (2007) Ontogenetic and temporal trajectories of chemical defense in a cyanogenic eucalypt. Oecologia, 153, 799-808.
26. Haase, D.L. & Rose, R. (1995) Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. Forest Science, 41, 54-66.
27. Hadfield, J.D., Richardson, D.S. & Burke, T. (2006) Towards unbiased parentage assignment: combining genetic, behavioral, and spatial data in a Bayesian framework. Molecular Ecology, 15, 3715-3730.
28. Hanley, M.E., Fenner, M., Whibley, H. & Darvill, B. (2004) Early plant growth: identifying the end of the seedling phase. New Phytologist, 163, 61-66.
29. Harper, J.L. (1977) Population Biology of Plants. Academic Press, London.
30. Hemming, J.D.C. & Lindroth, R.L. (1995) Intraspecific variation in aspen phytochemistry - effects on performance of gypsy moths and forest tent caterpillars. Oecologia, 103, 79-88.
31. Herman, J.J. & Sultan, S.E. (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science, 2, 1-10.
32. Herms, D.A. & Mattson, W.J. (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology, 67, 283-335.
33. Herrera, C.M. & Bazaga, P. (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Molecular Ecology, 20, 1675-1688.
34. Holeski, L.M. (2007) Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. Journal of Evolutionary Biology, 20, 2092-2100.
35. Holeski, L.M., Hillstrom, M.L., Whitham, T.G. & Lindroth, R.L. (2012) Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defense phenotype in a foundation tree species. Oecologia, 170, 695-704.
36. Holeski, L.M., Jander, G. & Agrawal, A.A. (2012) Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology and Evolution, 27, 618-626.
37. Hwang, S.Y. & Lindroth, R.L. (1998) Consequences of clonal variation in aspen phytochemistry for late season folivores. Ecoscience, 5, 508-516.
38. Iason, G. (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proceedings of the Nutrition Society, 64, 123-131.
39. Ivey, C.T., Carr, D.E. & Eubanks, M.D. (2009) Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus. Heredity, 102, 303-311.
40. Jablonka, E. & Raz, G. (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology, 84, 131-176.
41. Jaenisch, R. & Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics, 33, 245-254.
42. Karban, R. & Adler, F. (1996) Induced resistance to herbivores and the information content of early season attack. Oecologia, 107, 379-385.
43. Karban, R. & Baldwin, I.T. (1997) Induced defense and the evolution of induced resistance. Induced Responses to Herbivory (eds R. Karban & I.T. Baldwin ), pp. 167-204. The University of Chicago Press, Chicago, IL.
44. Karban, R., Agrawal, A.A., Thaler, J.S. & Adler, L.S. (1999) Induced plant responses and information content about risk of herbivory. Trends in Ecology and Evolution, 14, 443-447.
45. Kay, C.E. & Bartos, D.L. (2000) Ungulate herbivory on Utah aspen: assessment of long-termexclosures. Journal of Range Management, 53, 145-153.
46. Kearsley, M.J.C. & Whitham, T.G. (1992) Guns and butter: a no cost defense against predation for Chrysomela confluens. Oecologia, 92, 556-562.
47. Keim, P., Paige, K.N., Whitham, T.G. & Lark, K.G. (1989) Genetic analysis of an interspecific Hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics, 123, 557-565.
48. Koricheva, J. (1999) Interpreting phenotypic variation in plant phytochemistry: problems with the use of concentrations. Oecologia, 119, 467-473.
49. Koricheva, J. (2002) Meta-analysis of sources of variation in fitness costs of plant anti-herbivore defenses. Ecology, 83, 176-190.
50. Kruskal, J.B. (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika, 29, 1-26.
51. Lindroth, R.L., Hsia, M.T.S. & Scriber, J.M. (1987) Seasonal patterns in the phytochemistry of 3 Populus species. Biochemical Systematics and Ecology, 15, 681-686.
52. Marquis, R.J. (1992) Selective impact of herbivores. Plant Resistance to Herbivores and Pathogens (eds R.S. Fritz & E.L. Simms ), pp. 301-325. University of Chicago Press, Chicago, IL.
53. Martinsen, G.D., Whitham, T.G., Turek, R.J. & Keim, P. (2001) Hybrid populations selectively filter gene introgression between species. Evolution, 55, 1325-1335.
54. Mauricio, R. (1998) Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. American Naturalist, 151, 20-28.
55. Mauricio, R. & Rausher, M.D. (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution, 51, 1435-1444.
56. Mauricio, R., Rausher, M.D. & Burdick, D.S. (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology, 78, 1301-1311.
57. McKey, D. (1979) The distribution of secondary compounds within plants. Herbivores: Their Interaction with Secondary Plant Metabolites (eds G.A. Rosenthal & D.H. Janzen ), pp. 56-134. Academic Press, Orlando, FL.
58. Mosher, R.A. & Melnyk, C.W. (2011) siRNAs and DNA methylation: seedy epigenetics. Trends in Plant Science, 15, 204-210.
59. Mueller, R.C., Wade, B.D., Gehring, C.A. & Whitham, T.G. (2005) Chronic herbivory negatively impacts cone and seed production, seed quality, and seedling growth of susceptible pinyon pines. Oecologia, 143, 558-565.
60. Obeso, J.R. (1993) Does defoliation affect reproductive output in herbaceous perennials and woody plants in different ways? Functional Ecology, 7, 150-155.
61. Osier, T.L. & Lindroth, R.L. (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia, 148, 293-303.
62. Palo, R.T. (1984) Distribution of birch (Betula spp.), willow (Salix spp.), and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores. Journal of Chemical Ecology, 10, 499-520.
63. Pasteels, J.M., Rowellrahier, M., Braekman, J.C. & Dupont, A. (1983) Salicin from host plant as precursor of salicylaldehyde in defensive secretion of Chrysomeline larvae. Physiological Entomology, 8, 307-314.
64. Porter, L.J., Hrstich, L.N. & Chan, B.G. (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry, 25, 223-230.
65. Purrington, C.B. (2000) Costs of resistance. Current Opinion in Plant Biology, 3, 305-308.
66. R Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
67. Rasmann, S., De Vos, M., Casteel, C.L., Tian, D.L., Halitschke, R., Sun, J.Y., Agrawal, A.A., Felton, G.W., Jander, G. (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiology, 158, 854-863.
68. Rehill, B.J., Clauss, A., Wieczorek, L., Whitham, T.G. & Lindroth, R.L. (2005) Foliar phenolic glycosides from Populus fremontii, Populus angustifolia, and their hybrids. Biochemical Systematics and Ecology, 33, 125-131.
69. Rehill, B.J., Whitham, T.G., Martinsen, G.D., Schweitzer, J.A., Bailey, J.K. & Lindroth, R.L. (2006) Developmental trajectories in cottonwood phytochemistry. Journal of Chemical Ecology, 32, 2269-2285.
70. Richards, E.J. (2006) Inherited epigenetic variation-revisiting soft inheritance. Nature, 7, 395-401.
71. Rieseberg, L.H., Archer, M.A. & Wayne, R.K. (1999) Transgressive segregation, adaptation, and speciation. Heredity, 83, 363-372.
72. Roach, D.A. & Wulff, R.D. (1987) Maternal effects in plants. Annual Review of Ecology and Systematics, 18, 209-235.
73. Sampedro, L., Xoaquin, M. & Zas, R. (2011) Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. Journal of Ecology, 99, 818-827.
74. Scoville, A.G., Barnett, L.L., Bodbyl-Roels, S., Kelly, J.K. & Hileman, L.C. (2011) Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytologist, 191, 251-263.
75. Simonsen, A.K. & Stinchcombe, J.R. (2007) Induced responses in Ipomoea hederacea: simulated mammalian herbivory induces resistance and susceptibility to insect herbivores. Arthropod-Plant Interactions, 1, 129-136.
76. Smulders, M.J.M., Van Der Schoot, J., Arens, P. & Vosman, B. (2001) Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Molecular Ecology Notes, 1, 188-190.
77. Stamp, N. (2003) Out of the quagmire of plant defense hypotheses. The Quarterly Review of Biology, 78, 23-55.
78. Steets, J.A. & Ashman, T.-L. (2010) Maternal effects of herbivory in Impatiens capensis. International Journal of Plant Sciences, 171, 509-518.
79. Stevens, M.T., Waller, D.M. & Lindroth, R.L. (2007) Resistance and tolerance in Populus tremuloides: genetic variation, costs, and environmental dependency. Evolutionary Ecology, 21, 829-847.
80. Strauss, S.Y. & Agrawal, A.A. (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution, 14, 179-185.
81. Strauss, S.Y., Rudgers, J.A., Lau, J.A. & Irwin, R.E. (2002) Direct and ecological costs of resistance to herbivory. Trends in Ecology and Evolution, 17, 278-285.
82. Sultan, S.E., Barton, K. & Wilczek, A.M. (2009) Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology, 90, 1831-1839.
83. Thalmann, C., Freise, J., Heitland, W. & Bacher, S. (2003) Effects of defoliation by horse chestnut leafminer (Cameraria ohridella) on reproduction in Aesculus hippocastanum. Trees-Structure and Function, 17, 383-388.
84. Timmer, V.R. & Stone, E.L. (1978) Comparative foliar analysis of young balsam fir fertilized with nitrogen, phosphorous, potassium, and lime. Soil Science Society of America Journal, 42, 125-130.
85. Tuskan, G.A., Gunter, L.E., Yang, Z.K., Yin, T., Sewell, M.M. & Difazio, S.P. (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Canadian Journal of Forest Research, 34, 85-93.
86. Underwood, N.C. (1998) The timing of induced resistance and induced susceptibility in the soybean-Mexican bean beetle system. Oecologia, 114, 376-381.
87. Verhoeven, K.J.F. & van Gurp, T.P. (2012) Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS ONE, 7, e38605.
88. Verhoeven, K.J.F., Jansen, J.J., van Dijk, P.J. & Biere, A. (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist, 185, 1108-1118.
89. 2 generally have counteracting effects on phenolic phytochemistry of boreal trees? Journal of Chemical Ecology, 33, 287-296.
90. Waltz, A.M. & Whitham, T.G. (1997) Plant development affects arthropod communities: opposing impacts of species removal. Ecology, 78, 2133-2144.
91. Wang, J.L. (2004) Sibship reconstruction from genetic data with typing errors. Genetics, 166, 1963-1979.
92. Whitham, T.G. (1989) Plant hybrid zones as sinks for pests. Science, 244, 1490-1493.
93. Wooley, S.C., Walker, S., Vernon, J. & Lindroth, R.L. (2008) Aspen decline, aspen chemistry, and elk herbivory: are they linked? Rangelands, 30, 17-21.
94. Wulff, R.D. (1986) Seed size variation in Desmodium paniculatum. 1. Factors affecting seed size. Journal of Ecology, 74, 87-97.
95. Zangerl, A.R. (2003) Evolution of induced plant responses to herbivores. Basic and Applied Ecology, 4, 91-103.
96. Zangerl, A.R. & Berenbaum, M.R. (1990) Furanocoumarin induction in wild parsnip: genetics and populational variation. Ecology, 71, 1933-1940.