Journal of Chemical Ecology

, Volume 39, Issue 4, pp 525–536 | Cite as

Patterns of Phytochemical Variation in Mimulus guttatus (Yellow Monkeyflower)

  • Liza M. Holeski
  • Ken Keefover-Ring
  • M. Deane Bowers
  • Zoe T. Harnenz
  • Richard L. Lindroth
Article

Abstract

The search for general patterns in the production and allocation of plant defense traits will be facilitated by characterizing multivariate suites of defense, as well as by studying additional plant taxa, particularly those with available genomic resources. Here, we investigated patterns of genetic variation in phytochemical defenses (phenylpropanoid glycosides, PPGs) in Mimulus guttatus (yellow monkeyflower). We grew plants derived from several natural populations, consisting of multiple full-sibling families within each population, in a common greenhouse environment. We found substantial variation in the constitutive multivariate PPG phenotype and in constitutive levels of individual phytochemicals within plants (among leaves of different ages), within populations (among full-sibling families), and among populations. Populations consisting of annual plants generally, but not always, had lower concentrations of phytochemicals than did populations of perennial plants. Populations differed in their plastic response to artificial herbivory, both in the overall multivariate PPG phenotype and in the individual phytochemicals. The relationship between phytochemistry and another defense trait, trichomes, differed among populations. Finally, we demonstrated that one of the PPGs, verbascoside, acts as a feeding stimulant rather than a feeding deterrent for a specialist herbivore of M. guttatus, the buckeye caterpillar (Junonia coenia Nymphalidae). Given its available genetic resources, numerous, easily accessible natural populations, and patterns of genetic variation highlighted in this research, M. guttatus provides an ideal model system in which to test ecological and evolutionary theories of plant-herbivore interactions.

Keywords

Defense Genetic variation Junonia coenia Kairomone Mimulus guttatus Phenylpropanoid glycoside Model system 

Notes

Acknowledgments

The authors thank the Mimulus seed library (Duke University) and D. Lowry who generously provided some of the seeds used in this study. Thanks to E. Lewis and M. Crossley for help with sample processing and M. Arntz and R. Ecker for laboratory assistance. We are grateful for comments by several anonymous reviewers and J. Couture that substantially improved this manuscript. Z. HarnEnz was funded through the IBS-SRP (Integrated Biological Sciences Summer Research Program) at the University of Wisconsin, Madison. This work was supported in part by the National Science Foundation (grant numbers FIBR-0425908, DEB-0841609).

References

  1. Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85.CrossRefGoogle Scholar
  2. Agrawal, A. A. and Fishbein, M. 2006. Plant defense syndromes. Ecology 87:S132–S149.PubMedCrossRefGoogle Scholar
  3. Agrawal, A. A., Salminen, J.-H., and Fishbein, M. 2009. Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution 63:663–673.PubMedCrossRefGoogle Scholar
  4. Ali, J. G. and Agrawal, A. A. 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17:293–302.PubMedCrossRefGoogle Scholar
  5. Anderson, J. T. and Mitchell-Olds, T. 2011. Ecological genetics and genomics of plant defenses: evidence and approaches. Funct. Ecol. 25:312–324.PubMedCrossRefGoogle Scholar
  6. Barton, K. E. and Koricheva, J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 175:481–493.PubMedCrossRefGoogle Scholar
  7. Beardsley, P. M. and Olmstead, R. G. 2002. Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma. Am. J. Bot. 89:1093–1102.PubMedCrossRefGoogle Scholar
  8. Becerra, J. X., Noge, K., and Venable, D. L. 2009. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proc. Natl. Acad. Sci. U. S. A. 106:18062–18066.PubMedCrossRefGoogle Scholar
  9. Berenbaum, M. R. and Zangerl, A. 2008. Facing the future of plant-insect interaction research: Le retour a` la “raison d'être.”. Plant Physiol. 146:804–811.PubMedCrossRefGoogle Scholar
  10. Boege, K. and Marquis, R. J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:441–448.PubMedCrossRefGoogle Scholar
  11. Bowers, M. D. 1984. Iridoid glycosides and host-plant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567–1577.CrossRefGoogle Scholar
  12. Bowers, M. D. and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14:319–334.CrossRefGoogle Scholar
  13. Camara, M. D. 1997. Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable? J. Chem. Ecol. 23:2093–2106.CrossRefGoogle Scholar
  14. Carmona, D., Lajeunesse, M. J., and Johnson, M. T. J. 2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25:358–357.CrossRefGoogle Scholar
  15. Carr, D. E. and Eubanks, M. D. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Schrophulariaceae). Evolution 56:22–30.PubMedGoogle Scholar
  16. Carroll, M. J., Zangerl, A. R., and Berenbaum, M. R. 2000. Heritability estimates for octyl acetate and octyl butyrate in the mature fruit of the wild parsnip. J. Hered. 91:68–71.PubMedCrossRefGoogle Scholar
  17. Clauss, M. J., Dietel, S., Schubert, G., and Mitchell-Olds, T. 2006. Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. J. Chem. Ecol. 32:2351–2373.PubMedCrossRefGoogle Scholar
  18. Diezel, C., Ailmann, S., and Baldwin, I. T. 2011. Mechanisms of optimal defense patterns in Nicotiana attenuate: flowering attenuates herbivory-elicted ethylene and jasmonate signaling. J. Int. Plant Biol. 53:971–983.CrossRefGoogle Scholar
  19. Falconer, D. F. and Mackay, T. F. C. 1996. Introduction to Quantitative Genetics, 4th ed. Longman Group Ltd, England.Google Scholar
  20. Fenster, C. B. and Ritland, K. 1994. Quantitative genetics of mating system divergence in the yellow monkeyflower species complex. Heredity 73:422–435.CrossRefGoogle Scholar
  21. Franzyk, H., Husum, T. L., and Jensen, S. R. 1998. A caffeoyl phenylethanoid glycoside from Plantago myosuros. Phytochemistry 47:1161–1162.Google Scholar
  22. Geber, M. A. and Griffen, L. R. 2003. Inheritance and natural selection on functional traits. Int. J. Plant Sci. 164:S21–S42.CrossRefGoogle Scholar
  23. Hakes, A. S. and Cronin, J. T. 2011. Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): genetic variability, costs, and selection for multiple traits. Am. J. Bot. 98:1445–1455.CrossRefGoogle Scholar
  24. Hall, M. C. and Willis, J. H. 2006. Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60:2466–2477.PubMedGoogle Scholar
  25. Harborne, J. B. 1993. Introduction to Ecological Biochemistry, 4th ed. Academic, London.Google Scholar
  26. Hegnauer, R. and Kooiman, P. 1978. Taxonomic significance of iridoids of Tubiflorae sensu Wettstein. Planta Med. 33:1–33.PubMedCrossRefGoogle Scholar
  27. Hjältén, J. 2004. Simulating herbivory: problems and possibilities, pp. 243–255, in W. W. Weisser and E. Siemann (eds.), Ecological Studies-Analysis and Synthesis, Vol. 173. Springer-Verlag Press, Berlin.Google Scholar
  28. Holeski, L. M. 2007. Within and between generation variation in trichome density of Mimulus guttatus. J. Evol. Biol. 20:2092–2100.PubMedCrossRefGoogle Scholar
  29. Holeski, L. M., Chase-alone, R., and Kelly, J. K. 2010. The genetics of phenotypic plasticity in plant defense: trichome production in Mimulus guttatus. Am. Nat. 175:391–400.PubMedCrossRefGoogle Scholar
  30. Ivey, C. T., Carr, D. E., and 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.PubMedCrossRefGoogle Scholar
  31. Kelly, J. K. and Arathi, H. S. 2003. Inbreeding and the genetic variance in floral traits of Mimulus guttatus. Heredity 90:77–83.PubMedCrossRefGoogle Scholar
  32. Koricheva, J. 1999. Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 119:467–473.CrossRefGoogle Scholar
  33. Kruskal, J. B. 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–26.CrossRefGoogle Scholar
  34. Kursar, T. A. and Coley, P. D. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochem. Syst. Ecol. 8:929–949.CrossRefGoogle Scholar
  35. Lekberg, Y., Roskilly, B., Hendrick, M. F., Zabinkski, C. A., Barr, C. M., and Fishman, L. 2012. Phenotypic and genetic differentiation among yellow monkeyflower populations from thermal and non-thermal soils in Yellowstone National Park. Oecologia 170:111–122.PubMedCrossRefGoogle Scholar
  36. Levine, J. M. 1999. Indirect facilitation: evidence and predictions from a riparian community. Ecology 80:1762–1769.CrossRefGoogle Scholar
  37. Levine, J. M. 2000. Local interactions, dispersal, and native and exotic plant diversity along a California stream. Oikos 95:397–408.CrossRefGoogle Scholar
  38. Mitchell-Olds, T. 2001. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16:693–700.CrossRefGoogle Scholar
  39. Mølgaard, P. 1986. Population genetics and geographical distribution of caffeic acid esters in leaves of Plantago major in Denmark. J. Ecol. 74:1127–1137.CrossRefGoogle Scholar
  40. Mølgaard, P. and Ravn, H. 1988. Evolutionary aspects of caffeoyl ester distribution in dicotyledons. Phytochemistry 27:2411–2421.CrossRefGoogle Scholar
  41. Mousseau, T. A. and ROFF, D. A. 1987. Natural selection and the heritability of fitness components. Heredity 59:181–197.PubMedCrossRefGoogle Scholar
  42. Rausher, M. D. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12:212–217.PubMedCrossRefGoogle Scholar
  43. Reymond, P., Bodenhausen, N., van Poecke, R. M. P., Krisnamurthy, V., Dicke, M., and Farmer, E. E. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.PubMedCrossRefGoogle Scholar
  44. Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., and Manners, J. M. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. U. S. A. 97:11655–11660.PubMedCrossRefGoogle Scholar
  45. Stamp, N. 2003. Out of the quagmire of plant defense hypotheses. Quant. Rev. Biol. 78:23–55.CrossRefGoogle Scholar
  46. Stotz, H. U., Kroymann, J., and Mitchell-Olds, T. 1999. Plant-insect interactions. Curr. Opin. Plant Biol. 2:268–272.PubMedCrossRefGoogle Scholar
  47. Tian, D., Peiffer, M., Shoemaker, E., Tooker, J., Haubruge, E., Francis, F., Luthe, D. S., and Felton, D. W. 2012. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168.PubMedCrossRefGoogle Scholar
  48. van der Meijden, E., Wijn, M., and Verkaar, H. J. 1988. Defense and regrowth: alternative plant strategies in the struggle against herbivores. Oikos 51:355–363.CrossRefGoogle Scholar
  49. van der Putten, W. H. 2003. Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280.CrossRefGoogle Scholar
  50. Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W., and Willis, J. H. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100:220–230.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Liza M. Holeski
    • 1
  • Ken Keefover-Ring
    • 1
    • 2
  • M. Deane Bowers
    • 3
  • Zoe T. Harnenz
    • 1
    • 4
  • Richard L. Lindroth
    • 1
  1. 1.Department of EntomologyUniversity of WisconsinMadisonUSA
  2. 2.Department of Plant Physiology, Umeå Plant Science CentreUmeå UniversityUmeåSweden
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  4. 4.Integrated Biological Sciences Summer Research ProgramUniversity of WisconsinMadisonUSA

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