Journal of Chemical Ecology

, Volume 39, Issue 4, pp 516–524 | Cite as

Performance of an Herbivorous Leaf Beetle (Phratora vulgatissima) on Salix F2 Hybrids: the Importance of Phenolics

  • Mikaela TorpEmail author
  • Anna Lehrman
  • Johan A. Stenberg
  • Riitta Julkunen-Tiitto
  • Christer Björkman


The genotype of the plant determines, through the expression of the phenotype, how well it is suited as food for herbivores. Since hybridization often results in profound genomic alterations with subsequent changes in phenotypic traits, it has the potential to significantly affect plant-herbivore interactions. In this study, we used a population of F2 hybrids that originated from a cross between a Salix viminalis and a Salix dasyclados genotype, which differed in both phenolic content and resistance to the herbivorous leaf beetle Phratora vulgatissima. We screened for plants that showed a great variability in leaf beetle performance (i.e., oviposition and survival). By correlating leaf phenolics to the response of the herbivores, we evaluated the importance of different phenolic compounds for Salix resistance to the targeted insect species. The performance of P. vulgatissima varied among the F2 hybrids, and two patterns of resistance emerged: leaf beetle oviposition was intermediate on the F2 hybrids compared to the parental genotypes, whereas leaf beetle survival demonstrated similarities to one of the parents. The findings indicate that these life history traits are controlled by different resistance mechanisms that are inherited differently in the hybrids. Salicylates and a methylated luteolin derivative seem to play major roles in hybrid resistance to Phratora vulgatissima. Synergistic effects of these compounds, as well as potential threshold concentrations, are plausible. In addition, we found considerable variation in both distributions and concentrations of different phenolics in the F2 hybrids. The phenolic profiles of parental genotypes and F2 hybrids differed significantly (e.g., novel compounds appeared in the hybrids) suggesting genomic alterations with subsequent changes in biosynthetic pathways in the hybrids.


Hybridization Phenolics Luteolin Salicylates Phratora vulgatissima performance Resistance Salix 



We thank Elena Ahlbin, Marie Melander, Sussi Andersson Björkman, and Karin Eklund for assistance with insect bioassays and plant nursing, and Ann-Christin Rönnberg-Wästljung for advice and for providing plant material. This study was done as a part of the Salix Molecular Breeding Activities (SAMBA) project financed by the Swedish Energy Agency, the Faculty of Natural Resources and Agricultural Sciences at the Swedish University of Agricultural Sciences and Lantmännen Agroenergi AB.


  1. Arnold, M. L. 1997. Natural Hybridization and Evolution. Oxford University Press, New York.Google Scholar
  2. Barbehenn, R. V. and Constabel, C. P. 2011. Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565.PubMedCrossRefGoogle Scholar
  3. Baum, C., Toljander, Y. K., Eckhardt, K.-U., and Weih, M. 2009. The significance of host-fungus combinations in ectomycorrhizal symbioses for the chemical quality of willow foliage. Plant Soil 323:213–224.CrossRefGoogle Scholar
  4. Björkman, C., Höglund, S., Eklund, K., and Larsson, S. 2000. Effects of leaf beetle damage on stem wood production in coppicing willow. Agr. Forest Entomol. 2:131–139.CrossRefGoogle Scholar
  5. Boeckler, G. A., Gershenzon, J., and Unsicker, S. B. 2011. Phenolic glycosides of the Salicaceae and their role as anti-herbivore defences. Phytochemistry 72:1497–1509.PubMedCrossRefGoogle Scholar
  6. Cheng, D., Vrieling, K., and Klinkhamer, P. G. L. 2011. The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of chemical diversity in plants. Phytochem. Rev. 10:107–117.PubMedCrossRefGoogle Scholar
  7. Court, W. A., Brandle, J. E., Pocs, R., and Hendel, J. G. 1992. The chemical composition of somatic hybrids between Nicotiana tabacum and N. debneyi. Can. J. Plant Sci. 72:209–225.CrossRefGoogle Scholar
  8. Czesak, M. E., Knee, M. J., Gale, R. G., Bodach, S. D., and Fritz, R. S. 2004. Genetic architecture of resistance to aphids and mites in a willow hybrid system. Heredity 93:619–626.PubMedCrossRefGoogle Scholar
  9. Fahselt, D. and Ownbey, M. 1968. Chromatographic comparison of Dicentra species and hybrids. Am. J. Bot. 55:334–345.CrossRefGoogle Scholar
  10. Fraenkel, G. S. 1959. The raison d’être of secondary plant substances. Science 129:1466–1470.PubMedCrossRefGoogle Scholar
  11. Fritz, R. S. 1999. Resistance of hybrid plants to herbivores: genes, environment, or both? Ecology 80:382–391.CrossRefGoogle Scholar
  12. Fritz, R. S., Roche, B. M., and Brunsfeld, S. J. 1998. Genetic variation in resistance of hybrid willows to herbivores. Oikos 83:117–128.CrossRefGoogle Scholar
  13. Fritz, R. S., Moulia, C., and Newcombe, G. 1999. Resistance of hybrid plants and animals to herbivores, pathogens and parasites. Annu. Rev. Ecol. Syst. 30:565–91.CrossRefGoogle Scholar
  14. Glynn, C., Rönnberg-Wästljung, A.-C., Julkunen-Tiitto, R., and Weih, M. 2004. Willow genotype, but not drought treatment, affects foliar phenolic concentrations and leaf-beetle resistance. Entomol. Exp. Appl. 113:1–14.CrossRefGoogle Scholar
  15. Hallgren, P. 2003. Effects of willow hybridization and simulated browsing on the development and survival of the leaf beetle Phratora vitellinae. BMC Ecol. 3:5.PubMedCrossRefGoogle Scholar
  16. Hallgren, P., Ikonen, A., Hjältén, J., and Roininen, H. 2003. Inheritance patterns of phenolics in F1, F2, and back-cross hybrids of willows: implications for herbivore responses to hybrid plants. J. Chem. Ecol. 29:1143–1158.PubMedCrossRefGoogle Scholar
  17. Harborne, J. B. 2001. Twenty-five years of chemical ecology. Nat. Prod. Rep. 18:361–379.PubMedCrossRefGoogle Scholar
  18. Haukioja, E. 1980. On the role of plant defences in the fluctuation of herbivore populations. Oikos 35:202–213.CrossRefGoogle Scholar
  19. Hegarty, M. J., Barker, G. L., Brennan, A. C., Edwards, K. J., Abbott, R. J., and Hiscock, S. J. 2008. Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Philos. T. Roy. Soc. B 363:3055–3069.CrossRefGoogle Scholar
  20. Hjältén, J. 1998. An experimental test of hybrid resistance to insects and pathogens using Salix caprea, S. repens and their F1 hybrids. Oecologia 117:127–132.CrossRefGoogle Scholar
  21. Hjältén, J. and Hallgren, P. 2002. The resistance of hybrid willows to specialist and generalist herbivores and pathogens: the potential role of secondary chemistry and parent host plant status, pp. 153–168, in M. R. Wagner, K. M. Clancy, F. Lieutier, and T. D. Paine (eds.), Mechanisms and Deployment of Resistance in Trees to Insects. Kluwer Academic Publishers, New York.CrossRefGoogle Scholar
  22. Hochwender, C. G. and Fritz, R. S. 2004. Plant genetic differences influence herbivore community structure: evidence from a hybrid willow system. Oecologia 138:547–557.PubMedCrossRefGoogle Scholar
  23. Hochwender, C. G., Fritz, R. S., and Orians, C. M. 2000. Using hybrid systems to explore the evolution of tolerance to damage. Evol. Ecol. 14:509–521.CrossRefGoogle Scholar
  24. Julkunen-Tiitto, R. 1986. A chemotaxonomic survey of phenolics in leaves of northern Salicaceae species. Phytochemistry 25:663–667.CrossRefGoogle Scholar
  25. Julkunen-Tiitto, R. 1989. Phenolic constituents of Salix: a chemotaxonomic survey of further Finnish species. Phytochemistry 28:2115–2125.CrossRefGoogle Scholar
  26. Julkunen-Tiitto, R. and Sorsa, S. 2001. Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J. Chem. Ecol. 27:779–789.PubMedCrossRefGoogle Scholar
  27. Kelly, M. T. and Curry, J. P. 1991. The influence of phenolic compounds on the suitability of three Salix species as hosts for the willow beetle Phratora vulgatissima. Entomol. Exp. Appl. 61:25–32.CrossRefGoogle Scholar
  28. Kendall, D. A., Hunter, T., Arnold, G. M., Liggitt, J., Morris, T., and Wiltshire, C. W. 1996. Susceptibility of willow clones (Salix spp.) to herbivory by Phyllodecta vulgatissima (L.) and Galerucella lineola (Fab.) (Coleoptera, Chrysomelidae). Ann. Appl. Biol. 129:379–390.CrossRefGoogle Scholar
  29. Kirk, H., Vrieling, K., van der Meijden, E., and Klinkhamer, P. G. L. 2010. Species by environment interactions affect pyrrolizidine alkaloid expression in Senecio jacobaea, Senecio aquaticus, and their hybrids. J. Chem. Ecol. 36:378–387.PubMedCrossRefGoogle Scholar
  30. Lehrman, A., Torp, M., Stenberg, J. A., Julkunen-Tiitto, R., and Björkman, C. 2012. Estimating direct resistance in willows against a major insect pest (Phratora vulgatissima) comparing life history traits. Entomol. Exp. Appl. 144:93–100.CrossRefGoogle Scholar
  31. Matsuki, M. and MacLean Jr., S. F. 1994. Effects of different leaf traits on growth rates of insect herbivores on willows. Oecologia 100:141–152.CrossRefGoogle Scholar
  32. Mattson, W. J. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11:119–161.CrossRefGoogle Scholar
  33. Nahrung, H. F., Waugh, R., and Hayes, R. A. 2009. Corymbia species and hybrids: chemical and physical foliar attributes and implications for herbivory. J. Chem. Ecol. 35:1043–1053.PubMedCrossRefGoogle Scholar
  34. Nyman, T. and Julkunen-Tiitto, R. 2005. Chemical variation within and among six northern willow species. Phytochemistry 66:2836–2843.PubMedCrossRefGoogle Scholar
  35. Orians, C. M. 2000. The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant-herbivore interactions. Am. J. Bot. 87:1749–1756.PubMedCrossRefGoogle Scholar
  36. Orians, C. M. and Fritz, R. S. 1996. Genetic and soil-nutrient effects on the abundance of herbivores on willows. Oecologia 105:388–396.CrossRefGoogle Scholar
  37. Orians, C. M., Huang, C. H., Wild, A., Dorfman, K. A., Zee, P., Dao, M. T. T., and Fritz, R. S. 1997. Willow hybridization differentially affects preference and performance of herbivorous beetles. Entomol. Exp. Appl. 83:285–294.CrossRefGoogle Scholar
  38. Orians, C. M., Griffiths, M., Roche, B. M., and Fritz, R. S. 2000. Phenolic glycosides and condensed tannins in Salix sericea, S. eriocephala and their F1 hybrids: not all hybrids are created equal. Biochem. Syst. Ecol. 28:619–623.PubMedCrossRefGoogle Scholar
  39. Porter, L. J., Hrstich, L. N., and Chan, B. G. 1986. The conversation of proanthocyanidins and prodelohinidins to cyanidins and delphinidins. Phytochemistry 25:223–230.CrossRefGoogle Scholar
  40. Rebeiz, M., Jikomes, N., Kassner, V. A., and Carroll, S. B. 2011. Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. Proc. Natl. Acad. Sci. USA 108:10036–10043.PubMedCrossRefGoogle Scholar
  41. Rieseberg, L. H. and Ellstrand, N. C. 1993. What can molecular and morphological markers tell us about plant hybridization? Crit. Rev. Plant Sci. 12:213–241.Google Scholar
  42. Rowell-Rahier, M. 1984. The presence or absence of phenolglycosides in Salix (Salicaceae) leaves and the level of dietary specialization of some of their herbivorous insects. Oecologia 62:26–30.CrossRefGoogle Scholar
  43. Seigler, D. S. 1998. Plant Secondary Metabolism. Kluwer Academic Publishers, USA.Google Scholar
  44. Spring, O. and Schilling, E. E. 1989. Chemosystematic investigation of the annual species of Helianthus (Asteraceae). Biochem. Syst. Ecol. 17:519–528.CrossRefGoogle Scholar
  45. Stupar, R. M., Hermanson, P. J., and Springer, N. M. 2007. Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol. 145:411–425.PubMedCrossRefGoogle Scholar
  46. Tahvanainen, J., Julkunen-Tiitto, R., and Kettunen, J. 1985. Phenolic glucosides govern the food selection pattern of willow feeding leaf beetles. Oecologia 67:52–56.CrossRefGoogle Scholar
  47. Treutter, D. 2006. Significance of flavonoids in plant resistance: a review. Environ. Chem. Lett. 4:147–157.CrossRefGoogle Scholar
  48. Wang, J., Tian, L., Lee, H.-S., Wei, N. E., Jiang, H., Watson, B., Madlung, A., Osborn, T. C., Doerge, R. W., Comai, L., and Chen, Z. J. 2006. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517.PubMedCrossRefGoogle Scholar
  49. Whitham, T. G. 1989. Plant hybrid zones as sinks for pests. Science 244:1490–1493.CrossRefGoogle Scholar
  50. Yarnes, C. T., Boecklen, W. J., and Salminen, J. P. 2008. No simple sum: seasonal variation in tannin phenotypes and leaf-miners in hybrid oaks. Chemoecology 18:39–51.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Mikaela Torp
    • 1
    Email author
  • Anna Lehrman
    • 2
  • Johan A. Stenberg
    • 1
  • Riitta Julkunen-Tiitto
    • 3
  • Christer Björkman
    • 1
  1. 1.Department of EcologySwedish University of Agricultural SciencesUppsalaSweden
  2. 2.Department of Crop Production EcologySwedish University of Agricultural SciencesUppsalaSweden
  3. 3.Natural Product Research Laboratory, Department of BiologyUniversity of Eastern FinlandJoensuuFinland

Personalised recommendations