Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Feb 22;270(1513):357–366. doi: 10.1098/rspb.2002.2265

Variation in immune defence as a question of evolutionary ecology.

Paul Schmid-Hempel 1
PMCID: PMC1691258  PMID: 12639314

Abstract

The evolutionary-ecology approach to studying immune defences has generated a number of hypotheses that help to explain the observed variance in responses. Here, selected topics are reviewed in an attempt to identify the common problems, connections and generalities of the approach. In particular, the cost of immune defence, response specificity, sexual selection, neighbourhood effects and questions of optimal defence portfolios are discussed. While these questions still warrant further investigation, future challenges are the development of synthetic concepts for vertebrate and invertebrate systems and also of the theory that predicts immune responses based on a priori principles of evolutionary ecology.

Full Text

The Full Text of this article is available as a PDF (110.1 KB).

Selected References

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

  1. Anderson R. M., May R. M. Vaccination and herd immunity to infectious diseases. 1985 Nov 28-Dec 4Nature. 318(6044):323–329. doi: 10.1038/318323a0. [DOI] [PubMed] [Google Scholar]
  2. Barnard C. J., Behnke J. M., Sewell J. Environmental enrichment, immunocompetence, and resistance to Babesia microti in male mice. Physiol Behav. 1996 Nov;60(5):1223–1231. doi: 10.1016/s0031-9384(96)00174-6. [DOI] [PubMed] [Google Scholar]
  3. Barnes A. I., Siva-Jothy M. T. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc Biol Sci. 2000 Jan 22;267(1439):177–182. doi: 10.1098/rspb.2000.0984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bayyari G. R., Huff W. E., Rath N. C., Balog J. M., Newberry L. A., Villines J. D., Skeeles J. K., Anthony N. B., Nestor K. E. Effect of the genetic selection of turkeys for increased body weight and egg production on immune and physiological responses. Poult Sci. 1997 Feb;76(2):289–296. doi: 10.1093/ps/76.2.289. [DOI] [PubMed] [Google Scholar]
  5. Beegle C. C., Oatman E. R. Differential susceptibility of parasitized and nonparasitized larvae of Trichoplusia ni to a nuclear polyhedrosis virus. J Invertebr Pathol. 1974 Sep;24(2):188–195. doi: 10.1016/0022-2011(74)90010-x. [DOI] [PubMed] [Google Scholar]
  6. Boman H. G. Peptide antibiotics and their role in innate immunity. Annu Rev Immunol. 1995;13:61–92. doi: 10.1146/annurev.iy.13.040195.000425. [DOI] [PubMed] [Google Scholar]
  7. Brown P. Cinderella goes to the ball. Nature. 2001 Apr 26;410(6832):1018–1020. doi: 10.1038/35074279. [DOI] [PubMed] [Google Scholar]
  8. Carius H. J., Little T. J., Ebert D. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution. 2001 Jun;55(6):1136–1145. doi: 10.1111/j.0014-3820.2001.tb00633.x. [DOI] [PubMed] [Google Scholar]
  9. Chippindale A. K., Gibson J. R., Rice W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci U S A. 2001 Jan 30;98(4):1671–1675. doi: 10.1073/pnas.041378098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen J. E. Heterologous immunity in human malaria. Q Rev Biol. 1973 Sep;48(3):467–489. doi: 10.1086/407705. [DOI] [PubMed] [Google Scholar]
  11. De Boer R. J., Perelson A. S. How diverse should the immune system be? Proc Biol Sci. 1993 Jun 22;252(1335):171–175. doi: 10.1098/rspb.1993.0062. [DOI] [PubMed] [Google Scholar]
  12. Demas G. E., Chefer V., Talan M. I., Nelson R. J. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol. 1997 Nov;273(5 Pt 2):R1631–R1637. doi: 10.1152/ajpregu.1997.273.5.R1631. [DOI] [PubMed] [Google Scholar]
  13. Duckworth R. A., Mendonça M. T., Hill G. E. A condition dependent link between testosterone and disease resistance in the house finch. Proc Biol Sci. 2001 Dec 7;268(1484):2467–2472. doi: 10.1098/rspb.2001.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Engström Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev Comp Immunol. 1999 Jun-Jul;23(4-5):345–358. doi: 10.1016/s0145-305x(99)00016-6. [DOI] [PubMed] [Google Scholar]
  15. Fearon D. T., Locksley R. M. The instructive role of innate immunity in the acquired immune response. Science. 1996 Apr 5;272(5258):50–53. doi: 10.1126/science.272.5258.50. [DOI] [PubMed] [Google Scholar]
  16. Fellowes M. D., Godfray H. C. The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity (Edinb) 2000 Jan;84(Pt 1):1–8. doi: 10.1046/j.1365-2540.2000.00685.x. [DOI] [PubMed] [Google Scholar]
  17. Fellowes M. D., Kraaijeveld A. R., Godfray H. C. Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc Biol Sci. 1998 Aug 22;265(1405):1553–1558. doi: 10.1098/rspb.1998.0471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ferdig M. T., Beerntsen B. T., Spray F. J., Li J., Christensen B. M. Reproductive costs associated with resistance in a mosquito-filarial worm system. Am J Trop Med Hyg. 1993 Dec;49(6):756–762. doi: 10.4269/ajtmh.1993.49.756. [DOI] [PubMed] [Google Scholar]
  19. Ferrari J., Muller C. B., Kraaijeveld A. R., Godfray H. C. Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution. 2001 Sep;55(9):1805–1814. doi: 10.1554/0014-3820(2001)055[1805:CVACIA]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  20. Frank S. A. Specific and non-specific defense against parasitic attack. J Theor Biol. 2000 Feb 21;202(4):283–304. doi: 10.1006/jtbi.1999.1054. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Gray D. A. Sex differences in susceptibility of house crickets, acheta domesticus, to experimental infection with Serratia liquefaciens. J Invertebr Pathol. 1998 May;71(3):288–289. doi: 10.1006/jipa.1997.4742. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Haraguchi Y., Sasaki A. Evolutionary pattern of intra-host pathogen antigenic drift: effect of cross-reactivity in immune response. Philos Trans R Soc Lond B Biol Sci. 1997 Jan 29;352(1349):11–20. doi: 10.1098/rstb.1997.0002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Harvell C. D. The ecology and evolution of inducible defenses. Q Rev Biol. 1990 Sep;65(3):323–340. doi: 10.1086/416841. [DOI] [PubMed] [Google Scholar]
  26. Ilmonen P., Taarna T., Hasselquist D. Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc Biol Sci. 2000 Apr 7;267(1444):665–670. doi: 10.1098/rspb.2000.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Imler J. L., Hoffmann J. A. Signaling mechanisms in the antimicrobial host defense of Drosophila. Curr Opin Microbiol. 2000 Feb;3(1):16–22. doi: 10.1016/s1369-5274(99)00045-4. [DOI] [PubMed] [Google Scholar]
  28. Iwasa Y, Kubo T, van Dam N, de Jong TJ Optimal Level of Chemical Defense Decreasing with Leaf Age. Theor Popul Biol. 1996 Oct;50(2):124–148. doi: 10.1006/tpbi.1996.0026. [DOI] [PubMed] [Google Scholar]
  29. Jordan W. C., Bruford M. W. New perspectives on mate choice and the MHC. Heredity (Edinb) 1998 Sep;81(Pt 3):239–245. doi: 10.1038/sj.hdy.6884280. [DOI] [PubMed] [Google Scholar]
  30. Klasing K. C. Influence of acute feed deprivation or excess feed intake on immunocompetence of broiler chicks. Poult Sci. 1988 Apr;67(4):626–634. doi: 10.3382/ps.0670626. [DOI] [PubMed] [Google Scholar]
  31. Koella Jacob C., Boëte Christophe. A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution. 2002 May;56(5):1074–1079. doi: 10.1111/j.0014-3820.2002.tb01419.x. [DOI] [PubMed] [Google Scholar]
  32. Kraaijeveld A. R., Godfray H. C. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature. 1997 Sep 18;389(6648):278–280. doi: 10.1038/38483. [DOI] [PubMed] [Google Scholar]
  33. Kraaijeveld A. R., Limentani E. C., Godfray H. C. Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc Biol Sci. 2001 Feb 7;268(1464):259–261. doi: 10.1098/rspb.2000.1354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kurtz J., Wiesner A., Götz P., Sauer K. P. Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Dev Comp Immunol. 2000 Jan;24(1):1–12. doi: 10.1016/s0145-305x(99)00057-9. [DOI] [PubMed] [Google Scholar]
  35. Lacoste Arnaud, Malham Shelagh K., Gélébart Florence, Cueff Anne, Poulet Serge A. Stress-induced immune changes in the oyster Crassostrea gigas. Dev Comp Immunol. 2002 Jan;26(1):1–9. doi: 10.1016/s0145-305x(01)00067-2. [DOI] [PubMed] [Google Scholar]
  36. Lord G. M., Matarese G., Howard J. K., Baker R. J., Bloom S. R., Lechler R. I. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998 Aug 27;394(6696):897–901. doi: 10.1038/29795. [DOI] [PubMed] [Google Scholar]
  37. Lord G. M., Matarese G., Howard J. K., Lechler R. I. The bioenergetics of the immune system. Science. 2001 May 4;292(5518):855–856. doi: 10.1126/science.292.5518.855. [DOI] [PubMed] [Google Scholar]
  38. Matzinger Polly. The danger model: a renewed sense of self. Science. 2002 Apr 12;296(5566):301–305. doi: 10.1126/science.1071059. [DOI] [PubMed] [Google Scholar]
  39. McKean K. A., Nunney L. Increased sexual activity reduces male immune function in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2001 Jun 19;98(14):7904–7909. doi: 10.1073/pnas.131216398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Medzhitov R., Janeway C. A., Jr An ancient system of host defense. Curr Opin Immunol. 1998 Feb;10(1):12–15. doi: 10.1016/s0952-7915(98)80024-1. [DOI] [PubMed] [Google Scholar]
  41. Medzhitov Ruslan, Janeway Charles A., Jr Decoding the patterns of self and nonself by the innate immune system. Science. 2002 Apr 12;296(5566):298–300. doi: 10.1126/science.1068883. [DOI] [PubMed] [Google Scholar]
  42. Moret Y., Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science. 2000 Nov 10;290(5494):1166–1168. doi: 10.1126/science.290.5494.1166. [DOI] [PubMed] [Google Scholar]
  43. Møller A. P., Christe P., Lux E. Parasitism, host immune function, and sexual selection. Q Rev Biol. 1999 Mar;74(1):3–20. doi: 10.1086/392949. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Nappi A. J., Vass E. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res. 1993 Jun;6(3):117–126. doi: 10.1111/j.1600-0749.1993.tb00590.x. [DOI] [PubMed] [Google Scholar]
  46. Nestor K. E., Noble D. O., Zhu N. J., Moritsu Y. Direct and correlated responses to long-term selection for increased body weight and egg production in turkeys. Poult Sci. 1996 Oct;75(10):1180–1191. doi: 10.3382/ps.0751180. [DOI] [PubMed] [Google Scholar]
  47. Ots I., Hõrak P. Great tits Parus major trade health for reproduction. Proc Biol Sci. 1996 Nov 22;263(1376):1443–1447. doi: 10.1098/rspb.1996.0210. [DOI] [PubMed] [Google Scholar]
  48. Ots I., Kerimov A. B., Ivankina E. V., Ilyina T. A., Hõrak P. Immune challenge affects basal metabolic activity in wintering great tits. Proc Biol Sci. 2001 Jun 7;268(1472):1175–1181. doi: 10.1098/rspb.2001.1636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. doi: 10.1098/rspb.1997.0141. [DOI] [PMC free article] [Google Scholar]
  50. doi: 10.1098/rspb.1998.0400. [DOI] [PMC free article] [Google Scholar]
  51. doi: 10.1098/rspb.1998.0432. [DOI] [PMC free article] [Google Scholar]
  52. doi: 10.1098/rspb.1998.0481. [DOI] [PMC free article] [Google Scholar]
  53. doi: 10.1098/rspb.1999.0649. [DOI] [PMC free article] [Google Scholar]
  54. doi: 10.1098/rspb.1999.0650. [DOI] [PMC free article] [Google Scholar]
  55. doi: 10.1098/rspb.1999.0701. [DOI] [PMC free article] [Google Scholar]
  56. doi: 10.1098/rspb.1999.0750. [DOI] [PMC free article] [Google Scholar]
  57. Perelson A. S., Mirmirani M., Oster G. F. Optimal strategies in immunology. I. B-cell differentiation and proliferation. J Math Biol. 1976 Nov 25;3(3-4):325–367. doi: 10.1007/BF00275065. [DOI] [PubMed] [Google Scholar]
  58. Peters AD, Lively CM. The Red Queen and Fluctuating Epistasis: A Population Genetic Analysis of Antagonistic Coevolution. Am Nat. 1999 Oct;154(4):393–405. doi: 10.1086/303247. [DOI] [PubMed] [Google Scholar]
  59. Reusch T. B., Häberli M. A., Aeschlimann P. B., Milinski M. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature. 2001 Nov 15;414(6861):300–302. doi: 10.1038/35104547. [DOI] [PubMed] [Google Scholar]
  60. Richie T. L. Interactions between malaria parasites infecting the same vertebrate host. Parasitology. 1988 Jun;96(Pt 3):607–639. doi: 10.1017/s0031182000080227. [DOI] [PubMed] [Google Scholar]
  61. Richner H., Christe P., Oppliger A. Paternal investment affects prevalence of malaria. Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1192–1194. doi: 10.1073/pnas.92.4.1192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Rolff Jens. Bateman's principle and immunity. Proc Biol Sci. 2002 Apr 22;269(1493):867–872. doi: 10.1098/rspb.2002.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. 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]
  64. Råberg L., Grahn M., Hasselquist D., Svensson E. On the adaptive significance of stress-induced immunosuppression. Proc Biol Sci. 1998 Sep 7;265(1406):1637–1641. doi: 10.1098/rspb.1998.0482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Råberg Lars, Vestberg Mikael, Hasselquist Dennis, Holmdahl Rikard, Svensson Erik, Nilsson Jan-Ake. Basal metabolic rate and the evolution of the adaptive immune system. Proc Biol Sci. 2002 Apr 22;269(1493):817–821. doi: 10.1098/rspb.2001.1953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Schrag S. J., Perrot V., Levin B. R. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc Biol Sci. 1997 Sep 22;264(1386):1287–1291. doi: 10.1098/rspb.1997.0178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Shudo E., Iwasa Y. Inducible defense against pathogens and parasites: optimal choice among multiple options. J Theor Biol. 2001 Mar 21;209(2):233–247. doi: 10.1006/jtbi.2000.2259. [DOI] [PubMed] [Google Scholar]
  68. Söderhäll K., Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol. 1998 Feb;10(1):23–28. doi: 10.1016/s0952-7915(98)80026-5. [DOI] [PubMed] [Google Scholar]
  69. Wilson K. The costs of resistance in Drosophila: blood cells count. Trends Ecol Evol. 2001 Feb 1;16(2):72–73. doi: 10.1016/s0169-5347(00)02068-1. [DOI] [PubMed] [Google Scholar]
  70. Wilson Kenneth, Thomas Matthew B., Blanford Simon, Doggett Matthew, Simpson Stephen J., Moore Sarah L. Coping with crowds: density-dependent disease resistance in desert locusts. Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5471–5475. doi: 10.1073/pnas.082461999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Zasloff Michael. Antimicrobial peptides of multicellular organisms. Nature. 2002 Jan 24;415(6870):389–395. doi: 10.1038/415389a. [DOI] [PubMed] [Google Scholar]
  72. Zuk M., McKean K. A. Sex differences in parasite infections: patterns and processes. Int J Parasitol. 1996 Oct;26(10):1009–1023. [PubMed] [Google Scholar]
  73. von Schantz T., Wittzell H., Göransson G., Grahn M., Persson K. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc Biol Sci. 1996 Mar 22;263(1368):265–271. doi: 10.1098/rspb.1996.0041. [DOI] [PubMed] [Google Scholar]

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

RESOURCES