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Is there rapid evolutionary response in introduced populations of tansy ragwort, Jacobaea vulgaris, when exposed to biological control?

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Abstract

Differences in the herbivore community between a plant’s native (specialists and generalists) and introduced range (almost exclusively generalists) may lead to the evolution of reduced allocation to defences against specialist herbivores in the introduced range, allowing for increased allocation to competitive ability and to defences against generalist herbivores. Following this logic, the introduction of biological control agents should reverse this evolutionary shift and select for plants with life-history traits that are more similar to those of plants in the native range than those of plants in the introduced range that have not been exposed to biological control. In a common garden experiment, we compared performance and resistance traits of tansy ragwort, Jacobaea vulgaris, among populations from the introduced range (New Zealand and North America) that have either been exposed to or grown free from the biological control agent Longitarsus jacobaeae. For comparison, we included populations from the native European range. We found lower levels of generalist-deterrent pyrrolizidine alkaloids (PAs) and of soluble phenolics in New Zealand populations with than in populations without exposure to L. jacobaeae, while the opposite pattern was detected among North American populations. Contrary to expectation, populations with exposure to L. jacobaeae revealed more feeding damage by L. jacobaeae than populations without exposure. Introduced populations had higher levels of PAs and reproductive output than native J. vulgaris populations. Jacobaea vulgaris was introduced in different parts of the world some 100–130 years ago, while L. jacobaeae was introduced only some 20–40 years ago. Hence, the larger differences observed between native and introduced populations, as compared to introduced populations with and without biological control history, may result from different time scales available for selection to act.

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References

  • Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66

    Article  Google Scholar 

  • Bernays EA, Oppenheim S, Chapman RF, Kwon H, Gould F (2000) Taste sensitivity of insect herbivores to deterrents is greater in specialists than in generalists: a behavioral test of the hypothesis with two closely related caterpillars. J Chem Ecol 26:547–563

    Article  CAS  Google Scholar 

  • Bezemer TM, Harvey JA, Kowalchuk GA, Korpershoek H, van der Putten WH (2006) Community composition. Ecology 87:2002–2013

    Article  PubMed  Google Scholar 

  • Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Colautti RI, Maron JL, Barrett SCH (2009) Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evol Appl 2:187–199

    Article  Google Scholar 

  • Coombs EM, McEvoy PB, Turner CE (1999) Tansy Ragwort. In: Sheley RL, Petroff JK (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvallis, pp 389–400

    Google Scholar 

  • Coombs EM, McEvoy PB, Markin GP (2004) Tansy ragwort. In: Coombs EM, Clark JK, Piper GL, Cofrancesco AF Jr (eds) Biological control of invasive plants in the United States. Oregon State University Press, Corvallis, pp 337–345

    Google Scholar 

  • Crawley MJ (1983) Herbivory: the dynamics of animal-plant interactions. Berkeley, California

    Google Scholar 

  • Crutwell McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393

    Article  Google Scholar 

  • de Boer N (1999) Pyrrolizidine alkaloid distribution in Senecio jacobaea rosettes minimises losses to generalist feeding. Entomologia Experimentalis et Applicata 91:169–173

    Article  Google Scholar 

  • Dempster JP, Lakhani KH (1979) A population model for cinnabar moth and its food plant, ragwort. J Anim Ecol 48:143–163

    Article  Google Scholar 

  • Dietz H, Edwards PJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367

    Article  PubMed  Google Scholar 

  • Dobler S, Haberer W, Witte L, Hartmann T (2000) Selective sequestration of pyrrolizidine alkaloids from diverse host plants by Longitarsus flea beetles (Coleoptera, Chrysomelidae). J Chem Ecol 26:1281–1297

    Article  CAS  Google Scholar 

  • Elger A, Willby NJ (2003) Leaf dry matter content as an integrative expression of plant palatability: the case of freshwater macrophytes. Funct Ecol 17:58–65

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasion by animals and plants. Methuen, London

    Google Scholar 

  • Frick KE (1970) Ragwort flea beetle established for biological control of tansy ragwort in northern California. Calif Agric 24:12–13

    Google Scholar 

  • Frick KE (1972) Third list of insects that feed upon tansy ragwort Senecio jacobaea, in the Western United States. Ann Entomol Soc Am 65:629–631

    Google Scholar 

  • Handley RJ, Steinger T, Treier UA, Müller-Schärer H (2008) Regional differences in exposure-time to plant disease: testing the EICA hypothesis in a novel framework. Ecology 89:407–417

    Article  PubMed  Google Scholar 

  • Hanley ME, Lamont BB (2002) Relationship between physical and chemical attributes of congeneric seedlings: how important is seedling defence? Funct Ecol 16:216–222

    Article  Google Scholar 

  • Harper JL, Wood WA (1957) Senecio jacobaea L. J Ecol 45:617–637

    Article  Google Scholar 

  • Harris P, Wilkinson ATS, Neary ME, Thompson LS (1971) Senecio jacobaea L., tansy ragwort (Compositae). Commonw Inst Biol Control Tech Commun 4:97–104

    Google Scholar 

  • Hartmann T, Witte L (1995) Chemistry, biology and chemoecology of the pyrrolizidine alkaloids. In: Pelletier SW (ed) Alkaloids: chemical and biological perspectives, vol 9. Pergamon, New York, pp 156–233

    Google Scholar 

  • Hartmann T, Zimmer M (1986) Organ-specific distribution and accumulation of pyrrolizidine alkaloids during the life history of two annual Senecio species. J Plant Physiol 122:67–80

    CAS  Google Scholar 

  • Hayes LM (2000) Technology transfer programs for biological control of weeds—the New Zealand experience. In: Spencer NR (ed) Proceedings of the x international symposium on biological control of weeds. Montana State University, Bozeman, pp 719–727

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: To grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hinz HL, Schwarzlaender M (2004) Comparing invasive plants from their native and exotic range: what can we learn for biological control? Weed Technol 18:1533–1541

    Article  Google Scholar 

  • Isaacson DL (1973) Population dynamics of the cinnabar moth, Tyria jacobaea (Lepidoptera: Arctiidae). MSc thesis, Oregon State University, Corvallis

  • Isaacson DL (1978) Pacific Northwest Regional Commission land resource inventory demonstration project: inventory of the distribution and abundance of tansy ragwort in western Oregon. Oregon Department of Agriculture, Salem

    Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714

    Article  Google Scholar 

  • Julien MH, Griffiths MW (eds) (1998) Biological control of weeds: a world catalogue of agents and their target weeds, 4th edn. CAB International, Wallingford

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kirk H, Choi YH, Kim HK, Verpoorte R, van der Meijden E (2005) Comparing metabolomes: the chemical consequences of hybridization in plants. New Phytol 167:613–622

    Article  CAS  PubMed  Google Scholar 

  • Kollmann J, Banuelos MJ (2004) Latitudinal trends in growth and phenology of the invasive alien plant Impatiens glandulifera (Balsaminaceae). Divers Distrib 10:377–385

    Article  Google Scholar 

  • Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264

    Article  Google Scholar 

  • Leiss KA, Maltese F, Choi YH, Verpoorte R, Klinkhamer PGL (2009) Identification of chlorogenic acid as a resistance factor against thrips in Chrysanthemum. Plant Physiol 150:1567–1575

    Article  CAS  PubMed  Google Scholar 

  • Macel M, Vrieling K (2003) Pyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae. J Chem Ecol 29:1435–1446

    Article  CAS  PubMed  Google Scholar 

  • Macel M, Klinkhamer PGL, Vrieling K, van der Meijden E (2002) Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133:541–550

    Article  Google Scholar 

  • Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Maron JL, Vilà M (2008) Exotic plants in an altered enemy landscape: effects on enemy resistance. In: Kelley J, Tilmon J (eds) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 280–295

    Google Scholar 

  • Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • Maron JL, Elmendorf SC, Vilà M (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924

    Article  PubMed  Google Scholar 

  • McEvoy PB (1999) Biological control of plant invaders: regional patterns, field experiments, and structured population models. Ecol Appl 9:387–401

    Article  Google Scholar 

  • McEvoy PB, Cox CS, Coombs EM (1991) Successful biological control of ragwort, Senecio jacobaea, by introduced insects in Oregon. Ecol Appl 1:430–442

    Article  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  CAS  PubMed  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vázquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • Mitchell-Olds T (1996) Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50:1849–1858

    Article  Google Scholar 

  • Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biol Invasions 10:859–874

    Article  Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    Article  PubMed  Google Scholar 

  • Myers JH (1980) Is the insect or the plant the driving force in the cinnabar moth-tansy ragwort system? Oecologia 47:255–269

    Article  Google Scholar 

  • Pelser PB, Gravendeel B, van der Meijden R (2002) Tackling speciose genera: species composition and phylogenetic position of Senecio sect. Jacobaea (Asteraceae) based on plastid and nrDNA sequences. Am J Bot 89:929–939

    Article  CAS  Google Scholar 

  • Pelser PB, Veldkamp J-F, van der Meijden R (2006) New combinations in Jacobaea Mill (Asteracea-Senecioneae). Compos Newslett 44:1–11

    Google Scholar 

  • Pemberton RW, Turner CE (1990) Biological control of Senecio jacobaea in Northern California, an enduring success. Biocontrol 35:71–77

    Google Scholar 

  • Schaffner U, Vrieling K, van der Meijden E (2003) Pyrrolizidine alkaloid content in Senecio: ontogeny and developmental constraints. Chemoecology 13:39–46

    Article  CAS  Google Scholar 

  • Schoonhoven LM, Jermy T, van Loon JJA (1998) Insect-plant biology: from physiology to evolution. Chapman and Hall, London

    Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Stamp N, Osier TL (1998) Response of five insect herbivores to multiple allelochemicals under fluctuating temperatures. Entomologia Experimentalis et Applicata 88:81–96

    Article  CAS  Google Scholar 

  • Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37

    Article  Google Scholar 

  • Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101

    Article  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–284

    Article  Google Scholar 

  • Syrett P, Scheele SM, Philip BA (1984) Renewed activities in biological control of ragwort. In: 37th New Zealand weed and pest control conference, entomology division. DSIR, Lincoln, pp 37–41

  • Thomson GM (1922) The naturalisation of animals and plants in New Zealand. Cambridge University Press, London

    Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VG, Kurist AM (2003) Introduced species and their missing parasites. Nature 421:628–629

    Article  CAS  PubMed  Google Scholar 

  • van Dam NM, Vuister LWM, Bergshoeff C, de Vos H, van der Meijden E (1995) The “raison d’être” of pyrrolizidine alkaloids in Cynoglossum officinale: deterrent effects against generalist herbivores. J Chem Ecol 21:507–523

    Article  Google Scholar 

  • van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomologia Experimentalis et Applicata 80:307–310

    Article  Google Scholar 

  • van der Meijden E, van der Waals-Kooi RE (1979) The population ecology of Senecio jacobaea in a sand dune system. I. Reproductive strategy and the biennial habit. J Ecol 67:131–153

    Article  Google Scholar 

  • Vilà M, Gómez A, Maron JL (2003) Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia 137:211–215

    Article  PubMed  Google Scholar 

  • Vrieling K, de Boer N (1999) Host-plant choice and larval growth in the cinnabar moth: do pyrrolizidine alkaloids play a role? Entomologia Experimentalis et Applicata 91:251–257

    Article  CAS  Google Scholar 

  • Vrieling K, van Wijk CAM (1994) Cost assessment of the production of pyrrolizidine alkaloids in ragwort (Senecio jacobaea L.). Oecologia 97:541–546

    Article  Google Scholar 

  • Vrieling K, de Vos H, van Wijk CAM (1993) Genetic analysis of the concentrations of pyrrolizidine alkaloids in Senecio jacobaea. Phytochemistry 32:1141–1144

    Article  CAS  Google Scholar 

  • Weber E, Schmid B (1998) Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. Am J Bot 85:1110–1121

    Article  Google Scholar 

  • Wesselingh RA (1995) Ecology and genetics of reproductive timing in facultative biennial plants. PhD thesis, University of Leiden, Leiden, The Netherlands

  • Windig JJ (1993) Intensity of Longitarsus jacobaea herbivory and mortality of Senecio jacobaea. J Appl Ecol 30:179–186

    Article  Google Scholar 

  • Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proc Natl Acad Sci 102:15529–15532

    Article  CAS  PubMed  Google Scholar 

  • Zangerl AR, Stanley MC, Berenbaum MR (2008) Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist. Proc Natl Acad Sci 105:4547–4552

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to sincerely thank the many colleagues for collecting J. vulgaris seed material, N. Borowiec, R. Eschen, E. Gerber, N. Sailer, A. L. Torche and I. Vaisman for assistance in field and laboratory work, H. de Vos and C.A.M. van Wijk for their assistance in the chemical analyses, D. Matthies for statistical advice, and J. Maron, two anonymous referees and the handling editor for valuable comments on the manuscript. This research was financed by the National Centre of Competence in Research (NCCR) Plant Survival, research programme of the Swiss National Science Foundation to U.S. and H.M.S.

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Correspondence to Urs Schaffner.

Appendix

Appendix

See Tables 2 and 3.

Table 2 Origin of the populations of Jacobaea vulgaris included in the common garden experiment, and presence/absence of the biological control agent Longitarsus jacobaeae (in Chereng probably the sibling species L. flavicornis)
Table 3 Timetable of the experimental tasks carried out in each of the three experimental blocks

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Rapo, C., Müller-Schärer, H., Vrieling, K. et al. Is there rapid evolutionary response in introduced populations of tansy ragwort, Jacobaea vulgaris, when exposed to biological control?. Evol Ecol 24, 1081–1099 (2010). https://doi.org/10.1007/s10682-010-9367-4

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