Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Nov 7;270(1530):2257–2261. doi: 10.1098/rspb.2003.2472

The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle.

Markus J Rantala 1, Anssi Vainikka 1, Raine Kortet 1
PMCID: PMC1691508  PMID: 14613612

Abstract

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of mate quality because the hormones (e.g. testosterone) needed to develop secondary sexual traits have immunosuppressive effects. The best support for predictions arising from the immunocompetence handicap hypothesis so far comes from studies of insects, although they lack male-specific hormones such as testosterone. In our previous studies, we found that female mealworm beetles prefer pheromones of immunocompetent males. Here, we tested how juvenile hormone (JH) affects male investment in secondary sexual characteristics and immune functions in the mealworm beetle, Tenebrio molitor. We injected male mealworm beetles with JH (type III) and found that injection increased the attractiveness of male pheromones but simultaneously suppressed immune functions (phenoloxidase activity and encapsulation). Our results suggest that JH, which is involved in the control of reproduction and morphogenesis, also plays a central role in the regulation of a trade-off between the immune system and sexual advertisement in insects. Thus, the results reflect a general mechanism by which the immunocompetence handicap hypothesis may work in insects.

Full Text

The Full Text of this article is available as a PDF (134.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Clayton D. H. The influence of parasites on host sexual selection. Parasitol Today. 1991 Dec;7(12):329–334. doi: 10.1016/0169-4758(91)90211-6. [DOI] [PubMed] [Google Scholar]
  2. Gillespie J. P., Kanost M. R., Trenczek T. Biological mediators of insect immunity. Annu Rev Entomol. 1997;42:611–643. doi: 10.1146/annurev.ento.42.1.611. [DOI] [PubMed] [Google Scholar]
  3. Hamilton W. D., Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982 Oct 22;218(4570):384–387. doi: 10.1126/science.7123238. [DOI] [PubMed] [Google Scholar]
  4. Herman W. S., Tatar M. Juvenile hormone regulation of longevity in the migratory monarch butterfly. Proc Biol Sci. 2001 Dec 22;268(1485):2509–2514. doi: 10.1098/rspb.2001.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Kotiaho J. S. Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev Camb Philos Soc. 2001 Aug;76(3):365–376. doi: 10.1017/s1464793101005711. [DOI] [PubMed] [Google Scholar]
  6. Nappi A. J., Vass E., Frey F., Carton Y. Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur J Cell Biol. 1995 Dec;68(4):450–456. [PubMed] [Google Scholar]
  7. Nigam Y., Maudlin I., Welburn S., Ratcliffe N. A. Detection of phenoloxidase activity in the hemolymph of tsetse flies, refractory and susceptible to infection with Trypanosoma brucei rhodesiense. J Invertebr Pathol. 1997 May;69(3):279–281. doi: 10.1006/jipa.1996.4652. [DOI] [PubMed] [Google Scholar]
  8. Rantala M. J., Koskimäki J., Taskinen J., Tynkkynen K., Suhonen J. Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proc Biol Sci. 2000 Dec 7;267(1460):2453–2457. doi: 10.1098/rspb.2000.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Rantala Markus J., Jokinen Ilmari, Kortet Raine, Vainikka Anssi, Suhonen Jukka. Do pheromones reveal male immunocompetence? Proc Biol Sci. 2002 Aug 22;269(1501):1681–1685. doi: 10.1098/rspb.2002.2056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Rolff Jens, Siva-Jothy Michael T. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc Natl Acad Sci U S A. 2002 Jul 3;99(15):9916–9918. doi: 10.1073/pnas.152271999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ryder J. J., Siva-Jothy M. T. Male calling song provides a reliable signal of immune function in a cricket. Proc Biol Sci. 2000 Jun 22;267(1449):1171–1175. doi: 10.1098/rspb.2000.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Shiao S. H., Higgs S., Adelman Z., Christensen B. M., Liu S. H., Chen C. C. Effect of prophenoloxidase expression knockout on the melanization of microfilariae in the mosquito Armigeres subalbatus. Insect Mol Biol. 2001 Aug;10(4):315–321. doi: 10.1046/j.0962-1075.2001.00268.x. [DOI] [PubMed] [Google Scholar]
  13. Siva-Jothy M. T. A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc Biol Sci. 2000 Dec 22;267(1461):2523–2527. doi: 10.1098/rspb.2000.1315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Worden BD, Parker PG, Pappas PW. Parasites reduce attractiveness and reproductive success in male grain beetles. Anim Behav. 2000 Mar;59(3):543–550. doi: 10.1006/anbe.1999.1368. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES