Advertisement

Evolutionary Ecology

, Volume 24, Issue 6, pp 1307–1319 | Cite as

Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata

  • Nina SletvoldEmail author
  • Piritta Huttunen
  • Richard Handley
  • Katri Kärkkäinen
  • Jon Ågren
Article

Abstract

Theory predicts that trade-offs between resistance to herbivory and other traits positively affecting fitness can maintain genetic variation in resistance within plant populations. In the perennial herb Arabidopsis lyrata, trichome production is a resistance trait that exhibits both qualitative and quantitative variation. Using a paternal half-sib design, we conducted two greenhouse experiments to ask whether trichomes confer resistance to oviposition and leaf herbivory by the specialist moth Plutella xylostella, and to examine potential genetic constraints on evolution of increased resistance and trichome density. In addition, we examined whether trichome production is induced by insect herbivory. We found strong positive genetic and phenotypic correlations between leaf trichome density and resistance to leaf herbivory, demonstrating that the production of leaf trichomes increases resistance to leaf damage by P. xylostella. Also resistance to oviposition tended to increase with increasing leaf trichome density, but genetic and phenotypic correlations were not statistically significant. Trichome density and resistance to leaf herbivory were negatively correlated genetically with plant size in the absence of herbivores, but not in the presence of herbivores. There was no evidence of increased trichome production after leaf damage by P. xylostella. The results suggest that trichome production and resistance to leaf herbivory are associated with a cost and that the direction of selection on resistance and trichome density depends on the intensity of herbivory.

Keywords

Additive genetic variation Cost of resistance Herbivory Plant-animal interactions Resistance polymorphism Trichomes 

Notes

Acknowledgments

We thank M. Vallejo-Marin and two anonymous reviewers for helpful comments on the manuscript. This study was financially supported by grants from Formas and the Swedish Research Council to J.Å., from the Academy of Finland to P.H. and K.K., and from NorFA, the Finnish Cultural Foundation and the Evolutionary Ecology Graduate School of the University of Jyväskylä to P.H.

References

  1. Abdala-Roberts L, Parra-Tabla V (2005) Artificial defoliation induces trichome production in the tropical shrub Cnidoscolus aconitifolius (Euphorbiaceae). Biotropica 37:251–257CrossRefGoogle Scholar
  2. Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279:1201–1202CrossRefPubMedGoogle Scholar
  3. Agrawal AA (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723CrossRefGoogle Scholar
  4. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R (2002) Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–2213PubMedGoogle Scholar
  5. Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 259:89–120CrossRefGoogle Scholar
  6. Baucom RS, Mauricio R (2008) Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive. Evolution 62:2842–2854CrossRefPubMedGoogle Scholar
  7. Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558CrossRefGoogle Scholar
  8. Björkman C, Dalin P, Ahrne K (2008) Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytol 179:176–184CrossRefPubMedGoogle Scholar
  9. Clauss MJ, Dietel S, Schubert G, Mitchell-Olds T (2006) Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. J Chem Ecol 32:2351–2373CrossRefPubMedGoogle Scholar
  10. Dalin P, Björkman C (2003) Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia 134:112–118CrossRefPubMedGoogle Scholar
  11. Dalin P, Ågren J, Björkman C, Huttunen P, Kärkkäinen K (2008) Leaf trichome formation and plant resistance to herbivory. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Netherlands, pp 89–105CrossRefGoogle Scholar
  12. Elle E, Hare JD (2000) No benefit of glandular trichome production in natural populations of Datura wrightii? Oecologia 123:57–63CrossRefGoogle Scholar
  13. Hadfield JD, Wilson AJ, Garant D, Sheldon BC, Kruuk LEB (2010) The misuse of BLUP in ecology and evolution. Am Nat 175:116–125CrossRefPubMedGoogle Scholar
  14. Handley R, Ekbom B, Ågren J (2005) Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana. Ecol Entomol 30:284–292CrossRefGoogle Scholar
  15. Hare JD, Elle E (2004) Survival and seed production of sticky and velvety Datura wrightii in the field: a five-year study. Ecology 85:615–622CrossRefGoogle Scholar
  16. Hare JD, Elle E, van Dam NM (2003) Costs of glandular trichomes in Datura wrightii: a three-year study. Evolution 57:793–805PubMedGoogle Scholar
  17. Holeski LM (2007) Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. J Evol Biol 20:2092–2100CrossRefPubMedGoogle Scholar
  18. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204PubMedGoogle Scholar
  19. Hultén E (1971) Atlas of distribution of vascular plants in NW Europe. Generalstabens litografiska anstalt, Stockholm, SwedenGoogle Scholar
  20. Huttunen P, Kärkkäinen K, Løe G, Rautio P, Ågren J (2010) Leaf trichome production and response to defoliation and drought in Arabidopsis lyrata (Brassicaceae). Ann Bot Fenn (in press)Google Scholar
  21. Ivey CT, Carr DE, Eubanks MD (2009) Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus. Heredity 102:303–311CrossRefPubMedGoogle Scholar
  22. Jalas J, Suominen J (1994) Atlas Florae Europeae. Distribution of vascular plants in Europe. Helsinki University Printing House, HelsinkiGoogle Scholar
  23. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, IllGoogle Scholar
  24. Kärkkäinen K, Ågren J (2002) Genetic basis of trichome production in Arabidopsis lyrata. Hereditas 136:219–226CrossRefPubMedGoogle Scholar
  25. Kivimäki M, Kärkkäinen K, Gaudeul M, Løe G, Ågren J (2007) Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata. Mol Ecol 16:453–462CrossRefPubMedGoogle Scholar
  26. Koch MA, Matschinger M (2007) Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci 104:6272–6277CrossRefPubMedGoogle Scholar
  27. Koch MA, Wernisch M, Schmickl R (2008) Arabidopsis thaliana’s wild relatives: an updated overview on systematics, taxonomy and evolution. Taxon 57:933–943Google Scholar
  28. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190CrossRefGoogle Scholar
  29. Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15CrossRefGoogle Scholar
  30. Littell RC, Miliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS InstituteNC, CaryGoogle Scholar
  31. Løe G (2006) Ecology and evolution of resistance to herbivory. Dissertation, Uppsala UniversityGoogle Scholar
  32. Løe G, Toräng P, Gaudeul M, Ågren J (2007) Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata. Oikos 116:134–142CrossRefGoogle Scholar
  33. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  34. Mauricio R, Rausher MD (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444CrossRefGoogle Scholar
  35. Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Ann Rev Ecol Evol Syst 38:541–566CrossRefGoogle Scholar
  36. Reed DW, Pivnick KA, Underhill EW (1989) Identification of chemical oviposition stimulants for diamondback moth, Plutella xylostella, present in three species of Brassicaceae. Entomol Exp Appl 53:277–286CrossRefGoogle Scholar
  37. Sandring S, Ågren J (2009) Pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata. Evolution 63:1292–1300CrossRefPubMedGoogle Scholar
  38. Sandring S, Riihimäki M-A, Savolainen O, Ågren J (2007) Selection on flowering time and floral display in an alpine and a lowland population of Arabidopsis lyrata. J Evol Biol 20:558–567CrossRefPubMedGoogle Scholar
  39. Shaw RG, Platenkamp GAJ, Shaw FH, Podolsky RH (1995) Quantitative genetics of response to competitors in Nemophila menziesii–a field experiment. Genetics 139:397–406PubMedGoogle Scholar
  40. Simms E, Rausher M (1987) Costs and benefits of plant resistance to herbivory. Am Nat 130:570–581CrossRefGoogle Scholar
  41. Stevens MT, Waller DM, Lindroth RL (2007) Resistance and tolerance in Populus tremuloides: genetic variation, costs, and environmental dependency. Evol Ecol 21:829–847CrossRefGoogle Scholar
  42. Stinchcombe JR, Rausher MD (2001) Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea hederacea. Am Nat 158:376–388CrossRefPubMedGoogle Scholar
  43. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285CrossRefGoogle Scholar
  44. Talekar NS, Shelton AM (1993) Biology, ecology, and management of the diamondback moth. Ann Rev Entomol 38:275–301CrossRefGoogle Scholar
  45. Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716CrossRefPubMedGoogle Scholar
  46. Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532CrossRefGoogle Scholar
  47. Wise MJ (2007) Evolutionary ecology of resistance to herbivory: an investigation of potential genetic constraints in the multiple-herbivore community of Solanum carolinense. New Phytol 175:773–784CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Nina Sletvold
    • 1
    • 3
    Email author
  • Piritta Huttunen
    • 2
  • Richard Handley
    • 1
  • Katri Kärkkäinen
    • 2
  • Jon Ågren
    • 1
  1. 1.Plant Ecology, Department of Ecology and Evolution, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  2. 2.Finnish Forest Research InstituteMuhos Research UnitMuhosFinland
  3. 3.NTNU, Museum of Natural History and ArchaeologyTrondheimNorway

Personalised recommendations