Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Host recognition by the tobacco hornworm is mediated by a host plant compound

Abstract

It is generally believed that animals make decisions about the selection of mates, kin or food on the basis of pre-constructed recognition templates. These templates can be innate or acquired through experience1. An example of an acquired template is the feeding preference exhibited by larvae of the moth, Manduca sexta. Naive hatchlings will feed and grow successfully on many different plants or artificial diets, but once they have fed on a natural host they become specialist feeders2,3,4,5,6. Here we show that the induced feeding preference of M. sexta involves the formation of a template to a steroidal glycoside, indioside D, that is present in solanaceous foliage. This compound is both necessary and sufficient to maintain the induced feeding preference. The induction of host plant specificity is at least partly due to a tuning of taste receptors to indioside D. The taste receptors of larvae fed on host plants show an enhanced response to indioside D as compared with other plant compounds tested.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Host-restricted feeding behaviour is determined by dietary experience.
Figure 2: Indioside D is a recognition cue for host-restricted larvae.
Figure 3: The lateral sensilla styloconia of host-restricted larvae are tuned to indioside D.

References

  1. Sherman, P. W., Reeve, H. K. & Pfenning, D. W. in Behavioral Ecology An Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 69–96 (Blackwell Science, Oxford, 1997).

    Google Scholar 

  2. Schoonhoven, L. M. Loss of host plant specificity by Manduca sexta after rearing on an artificial diet. Entomol. Exp. Appl. 10, 270–272 (1967).

    Article  Google Scholar 

  3. Jermy, T., Hanson, F. E. & Dethier, V. G. Induction of specific food preference in lepidopterous larvae. Entomol. Exp. Appl. 47, 211–230 (1967).

    Google Scholar 

  4. Yamamoto, R. T. & Fraenkel, G. S. The specificity of the tobacco hornworm, Protoparce sexta, to solanaceous plants. Ann. Entomol. Soc. Am. 53, 503–507 (1960).

    Article  Google Scholar 

  5. Yamamoto, R. T. Induction of hostplant specificity in the tobacco hornworm, Manduca sexta. J. Insect Physiol. 20, 641–650 (1974).

    Article  Google Scholar 

  6. Mechaber, W. L. & Hildebrand, J. G. Novel non-solanaceous host plant record for Manduca sexta (Lepidoptera: Sphingidae) in the southwestern United States. Ann. Entomol. Soc. Am. 93, 447–451 (2000).

    Article  Google Scholar 

  7. Bell, R. A., Owens, C. D., Shapiro, M. & Tardif, J. R. in The Gypsy Moth: Research Toward Integrated Pest Management. (eds Doane, C. C. & McManus, M. L.) 599–633 (USDA-FS Technical Bulletin 1584 (Washington DC, 1981).

    Google Scholar 

  8. Croasmun, W. A. & Carlson, R. M. K. (eds) Two-Dimentional NMR spectroscopy. Applications for Chemists and Biochemists 2nd edn (VCH, New York, 1994).

    Google Scholar 

  9. Yajara, S. et al. Steroidal glycosides, indiosides A–E, from Solanum indicum. Phytochemistry 43, 1319–1323 (1996).

    Article  Google Scholar 

  10. Dethier, V. G. & Crnjar, R. M. Candidate codes in the gustatory system of caterpillars. J. Gen. Physiol. 79, 549–569 (1982).

    CAS  Article  Google Scholar 

  11. Bernays, E. A. Selective attention and host-plant specialization. Entomol. Exp. Appl. 80, 125–131 (1996).

    Article  Google Scholar 

  12. Waldbauer, G. P. & Fraenkel, G. Feeding on normally rejected plants by maxillectomized larvae of the tobacco hornworm, Protoparce sexta (Lepidoptera, Sphingidae). Ann. Ent. Soc. Am. 54, 477–485 (1961).

    Article  Google Scholar 

  13. de Boer, G. Role of bilateral chemosensory input in food discrimination by Manduca sexta. Entomol. Exp. Appl. 61, 159–168 (1991).

    Article  Google Scholar 

  14. de Boer, G. Effect of diet experience on the ability of different larval chemosensory organs to mediate food discrimination by the tobacco hornworm, Manduca sexta. J. Insect Physiol. 37, 763–769 (1991).

    Article  Google Scholar 

  15. Flowers, R. W. & Yamamoto, R. T. Feeding on non-host plants by partially maxillectomized tobacco hornworms (Manduca sexta: Lepidoptera: Sphingidae). Florida Entomol. 75, 89–93 (1992).

    Article  Google Scholar 

  16. de Boer, G. Plasticity in food preference and diet-induced differential weighting of chemosensory information in larval Manduca sexta. J. Insect Physiol. 12, 17–24 (1993).

    Article  Google Scholar 

  17. Schoonhoven, L. M. & Dethier, V. G. Sensory aspects of host plant discrimination by lepidopterous larvae. Arch. Neder. Zool. 16, 497–530 (1966).

    Google Scholar 

  18. Schoonhoven, L. M. Sensitivity changes in some insect chemoreceptors and their effect on food selection behavior. Proc. K. Ned. Akad. Wet. C 72, 491–498 (1969).

    Google Scholar 

  19. Städler, E. & Hanson, F. E. in Host Plant in Relation to Insect Behavior and Reproduction (ed. Jermy, T.) 267–273 (Plenum, New York, 1976).

    Book  Google Scholar 

  20. Abisgold, J. D. & Simpson, S. J. The effect of dietary protein levels and haemolymph composition on the sensitivity of maxillary palp chemoreceptors of locusts. J. Exp. Biol. 135, 215–229 (1988).

    CAS  Google Scholar 

  21. Glendinning, J. I., Ensslen, S., Eisenberg, E. & Weiskopf, P. Diet-induced plasticity in the taste system of an insect: localization to a single transduction pathway in an identified taste cell. J. Exp. Biol. 202, 2091–2102 (1999).

    CAS  Google Scholar 

  22. Rothschild, M., Aplin, R. & Marsh, N. Toxicity induced in the tobacco horn-worm (Manduca sexta L. ) (Sphingidae, Lepidoptera). Nature 280, 487–488 (1979).

    ADS  CAS  Article  Google Scholar 

  23. Gothilf, S. E. & Hanson, F. E. Technique for electrophysiologically recording from sensory organs of intact caterpillars. Entomol. Axp. Appl. 72, 305–310 (1994).

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Ewer, K. Whitlock, D. Bodnar, C. Gilbert, P. Rivlin and J. Bestman for critical reviews of the manuscript; M. Haribal for preliminary NMR and MS; B. Johnson for equipment to analyse electrophysiological recordings; and J. Almadovar and M. Chu for help in the laboratory. This work was supported by grants from the NSF and the Binational Science Foundation to R.B., and the NSF to C.I.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marta L. del Campo.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

del Campo, M., Miles, C., Schroeder, F. et al. Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411, 186–189 (2001). https://doi.org/10.1038/35075559

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35075559

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing