Skip to main content

Inter- and Intrapopulation Variability in the Composition of Larval Defensive Secretions of Willow-Feeding Populations of the Leaf Beetle Chrysomela lapponica

Abstract

We explored the inter- and intrapopulation variability in the larval defensive chemistry of the leaf beetle Chrysomela lapponica with respect to the salicylic glycoside (SG) content of its host species. Secretions of larvae from three populations associated in nature with SG-poor willows contained nearly twice as many components and 40-fold higher concentrations of autogenously produced isobutyrates and 2-methylbutyrates than secretions of larvae from three populations associated with SG-rich willows, which in turn had 200-fold higher concentrations of host-derived salicylaldehyde. Reciprocal transfer experiments showed that the larvae from populations associated with SG-rich willows did not produce appreciable amounts of butyrates on either SG-rich or SG-poor willows, while populations feeding on several SG-poor willow species retained the ability for efficient sequestration of SGs, along with their ability to produce high amounts of isobutyrates and 2-methylbutyrates. Only the populations associated with SG-poor willows demonstrated among-family variation in the composition of defensive secretion and differential responses of individual families to willows with alternative SG levels, which can be seen as the prerequisites for shifting to novel hosts. These non-specialized populations show a dual defensive strategy, which corresponds to the ancestral state of this species, while populations that fully depend on host-derived toxins (feeding on SG-rich willows) or have lost the ability to produce salicylaldehyde (feeding on birches) are most deviant from the ancestral state. The results indicate that defensive strategies may differ between populations within a species, and suggest that this variation reduces extinction risks and maintains the high ecological diversity and wide distribution of C. lapponica.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Becerra JX (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256

    Article  CAS  PubMed  Google Scholar 

  • Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Blum MS, Brand JM, Wallace JB, Fales HM (1972) Chemical characterization of defensive secretion of a chrysomelid larva. Life Sci 11:525–531

    Article  CAS  Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • Brückmann M, Termonia A, Pasteels JM, Hartmann T (2002) Characterization of an extracellular salicyl alcohol oxidase from larval defensive secretions of Chrysomela populi and Phratora vitellinae (Chrysomelina). Insect Biochem Mol Biol 32:1517–1523

    Article  PubMed  Google Scholar 

  • Denno RF, Larsson S, Olmstead KL (1990) Role of enemy free space and plant quality in host plant selection by willow beetles. Ecology 71:124–137

    Article  Google Scholar 

  • Eggenberger F, Rowell-Rahier M (1992) Genetic component of variation in chemical defense of Oreina gloriosa (Coleoptera, Chrysomelidae). J Chem Ecol 18:1375–1404

    Article  CAS  PubMed  Google Scholar 

  • Fox LR, Morrow PA (1981) Specialization: species property or local phenomenon? Science 211:887–893

    Article  CAS  PubMed  Google Scholar 

  • Funk DJ, Futuyma DJ, Orti G, Meyer A (1995) A history of host associations and evolutionary diversification for Ophraella (Coleoptera, Chrysomelidae) – new evidence from mitochondrial DNA. Evolution 49:1008–1017

    Article  CAS  Google Scholar 

  • Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci U S A 106:18054–18061

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Futuyma DJ, McCafferty SS (1990) Phylogeny and the evolution of host plant associations in the leaf beetle genus Ophraella (Coleoptera, Chrysomelidae). Evolution 44:1885–1913

    Article  Google Scholar 

  • Gross J, Hilker M (1995) Chemoecological studies of the exocrine glandular larval secretions of two chrysomelid species (Coleoptera): Phaedon cochleariae and Chrysomela lapponica. Chemoecology 5:185–189

    Google Scholar 

  • Gross J, Podsiadlowski L, Hilker M (2002) Antimicrobial activity of exocrine glandular secretion of Chrysomela larvae. J Chem Ecol 28:317–331

    Article  CAS  PubMed  Google Scholar 

  • Gross J, Fatouros NE, Hilker M (2004a) The significance of bottom-up effects for host plant specialization in Chrysomela leaf beetles. Oikos 105:368–376

    Article  Google Scholar 

  • Gross J, Fatouros NE, Neuvonen S, Hilker M (2004b) The importance of specialist natural enemies for Chrysomela lapponica in pioneering a new host plant. Ecol Entomol 29:584–593

    Article  Google Scholar 

  • Gross J, Fatouros NE, Neuvonen S, Hilker M (2007) The role of competitors for Chrysomela lapponica, a north Eurasian willow pest, in pioneering a new host plant. J Pest Sci 80:139–143

    Article  Google Scholar 

  • Hilker M, Schulz S (1994) Composition of larval secretion of Chrysomela lapponica (Coleoptera, Chrysomelidae) and its dependence on host-plant. J Chem Ecol 20:1075–1093

    Article  CAS  PubMed  Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jones CG, Hess TA, Whitman DW, Silk PJ, Blum MS (1986) Idiosyncratic variation in chemical defenses among individual generalist grasshoppers. J Chem Ecol 12:749–761

    Article  CAS  PubMed  Google Scholar 

  • Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92

    Article  Google Scholar 

  • Julkunen-Tiitto R (1989) Phenolic constituents of Salix: a chemotaxonomic survey of further Finnish species. Phytochemistry 28:2115–2125

    Article  CAS  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kelley ST, Farrell BD (1998) Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolitidae). Evolution 52:1731–1743

    Article  CAS  Google Scholar 

  • Kirsch R, Vogel H, Muck A, Reichwald K, Pasteels JM, Boland W (2011) Host plant shifts affect a major defense enzyme in Chrysomela lapponica. Proc Natl Acad Sci U S A 108:4897–4901

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kuhn J, Pettersson EM, Feld BK, Burse A, Termonia A, Pasteels JM, Boland W (2004) Selective transport systems mediate sequestration of plant glucosides in leaf beetles: a molecular basis for adaptation and evolution. Proc Natl Acad Sci U S A 101:13808–13813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute Inc., Cary

    Google Scholar 

  • Loxdale HD, Lushai G, Harvey JA (2011) The evolutionary improbability of ‘generalism’ in nature, with special reference to insects. Biol J Linn Soc 103:1–18

    Article  Google Scholar 

  • Lundvall P, Neuvonen S, Halonen M (1998) Interspecific differences in the susceptibility of adult leaf beetles (Col., Chrysomelidae) to predation by willow warblers (Phylloscopus trochilus). Rep Kevo Subarctic Res Station 22:19–24

    Google Scholar 

  • Machkour-M’Rabet S, Mardulyn P, Pasteels JM (2008) Genetic differentiation among European samples of the arctic-alpine leaf beetle, Chrysomela lapponica. Entomol Exp Appl 129:181–188

    Article  Google Scholar 

  • Mardulyn P, Othmezouri N, Mikhailov YE, Pasteels JM (2011) Conflicting mitochondrial and nuclear phylogeographic signals and evolution of host-plant shifts in the boreo-montane leaf beetle Chrysomela lapponica. Mol Phylogenet Evol 61:686–696

    Article  PubMed  Google Scholar 

  • Mayr E (1963) Animal Species and Evolution. Harvard Univ Press, Cambridge

    Book  Google Scholar 

  • Messina FJ, Durham SL (2013) Adaptation to a novel host by a seed beetle (Coleoptera: Chrysomelidae: Bruchinae): effect of source population. Environ Entomol 42:733–742

    Article  PubMed  Google Scholar 

  • Michalski C, Mohagheghi H, Nimtz M, Pasteels J, Ober D (2008) Salicyl alcohol oxidase of the chemical defensive secretion of two chrysomelid leaf beetles: molecular and functional characterization of two new members of the glucose-methanol-choline oxidoreductase gene family. J Biol Chem 283:19219–19228

    Article  CAS  PubMed  Google Scholar 

  • Novak D, Pflanzer F (1982) Versuche mit einigen neuen Repellents gegen Pharaoameisen. Angew Parasitol 23:47–48

    CAS  PubMed  Google Scholar 

  • Pasteels JM, Braekman JC, Daloze D, Ottinger R (1982) Chemical defence in chrysomelid larvae and adults. Tetrahedron 38:1891–1897

    Article  CAS  Google Scholar 

  • Pasteels JM, Gregoire JC, Rowell-Rahier M (1983a) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:263–289

    Article  CAS  Google Scholar 

  • Pasteels JM, Rowell-Rahier M, Braekman JC, Dupont A (1983b) Salicin from host plant as precursor of salicylaldehyde in defensive secretion of chrysomeline larvae. Physiol Entomol 8:307–314

    Article  CAS  Google Scholar 

  • Pavan M (1953) Antibiotics and insecticides of animal origin. I. The active principle of the larva of Melasoma populi. Arch Zool Ital 38:157–184

    CAS  Google Scholar 

  • SAS Institute (2009) SAS/Stat. User's Guide, Version 9.2. SAS Institute, Cary SAS Institute (2009) SAS/Stat. User's Guide, Version 9.2. SAS Institute, Cary

  • Schulz S, Gross J, Hilker M (1997) Origin of the defensive secretion of the leaf beetle Chrysomela lapponica. Tetrahedron 53:9203–9212

    Article  CAS  Google Scholar 

  • Speed MP, Ruxton GD, Mappes J, Sherratt TN (2012) Why are defensive toxins so variable? An evolutionary perspective. Biol Rev 87:874–884

    Article  PubMed  Google Scholar 

  • Termonia A, Pasteels JM (1999) Larval chemical defense and evolution of host shifts in Chrysomela leaf beetles. Chemoecology 9:13–23

    Article  CAS  Google Scholar 

  • Termonia A, Hsiao TH, Pasteels JM, Milinkovitch MC (2001) Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end. Proc Natl Acad Sci U S A 98:3909–3914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tilmon KJ, Wood TK, Pesek JD (1998) Genetic variation in performance traits and the potential for host shifts in Enchenopa treehoppers (Homoptera: Membracidae). Ann Entomol Soc Am 91:397–403

    Article  Google Scholar 

  • Tolzin-Banasch K, Dagvadorj E, Sammer U, Kunert M, Kirsch R, Ploss K, Pasteels JM, Boland W (2011) Glucose and glucose esters in the larval secretion of Chrysomela lapponica; selectivity of the glucoside import system from host plant leaves. J Chem Ecol 37:195–204

    Article  CAS  PubMed  Google Scholar 

  • Yezerski A, Gilmor TP, Stevens L (2000) Variation in the production and distribution of substituted benzoquinone compounds among genetic strains of the confused flour beetle, Tribolium confusum. Physiol Biochem Zool 73:192–199

    Article  CAS  PubMed  Google Scholar 

  • Zvereva EL, Kozlov MV (2000) Natural enemies of the leaf beetle, Melasoma lapponica, in the impact zone of a nickel-copper smelter: density dependence and effects of air pollution. J Appl Ecol 37:298–308

    Article  Google Scholar 

  • Zvereva EL, Rank NE (2003) Host-plant effects on parasitoid attack on the leaf beetle, Chrysomela lapponica. Oecologia 135:258–267

    Article  CAS  PubMed  Google Scholar 

  • Zvereva EL, Rank NE (2004) Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140:516–522

    Article  CAS  PubMed  Google Scholar 

  • Zvereva EL, Kozlov MV, Kruglova OY (2002) Color polymorphism in relation to population dynamics of the leaf beetle Chrysomela lapponica. Evol Ecol 16:523–539

    Article  Google Scholar 

  • Zvereva EL, Kozlov MV, Hilker M (2010a) Evolutionary variation on a theme: host plant specialization in five geographical populations of the leaf beetle Chrysomela lapponica. Popul Ecol 52:389–396

    Article  Google Scholar 

  • Zvereva EL, Kruglova OY, Kozlov MV (2010b) Drivers of host plant shifts in the leaf beetle Chrysomela lapponica: natural enemies or competition? Ecol Entomol 35:611–622

    Article  Google Scholar 

Download references

Acknowledgments

We thank V. Zverev, O. Kruglova, and S. Didorenko for assistance in collecting material, V. Chepinoga for identification of plant species from Baikal, T. Klemola for statistical advices, and two anonymous reviewers for comments to an earlier version of the manuscript. The study was supported by the Academy of Finland (projects 122133 and 268124, researcher exchange grants to E. Zvereva and researcher post of M. Kozlov) and by a strategic research grant from the University of Turku.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elena L. Zvereva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(XLS 236 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Geiselhardt, S., Hilker, M., Müller, F. et al. Inter- and Intrapopulation Variability in the Composition of Larval Defensive Secretions of Willow-Feeding Populations of the Leaf Beetle Chrysomela lapponica . J Chem Ecol 41, 276–286 (2015). https://doi.org/10.1007/s10886-015-0558-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0558-x

Keywords

  • Esters
  • Host shift
  • Local adaptation
  • Salicylaldehyde
  • Salix caprea
  • Salix myrsinifolia
  • Coleoptera
  • Chrysomelidae