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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Apr 22;269(1493):817–821. doi: 10.1098/rspb.2001.1953

Basal metabolic rate and the evolution of the adaptive immune system.

Lars Råberg 1, Mikael Vestberg 1, Dennis Hasselquist 1, Rikard Holmdahl 1, Erik Svensson 1, Jan-Ake Nilsson 1
PMCID: PMC1690958  PMID: 11958713

Abstract

Vertebrates have evolved an adaptive immune system in addition to the ancestral innate immune system. It is often assumed that a trade-off between costs and benefits of defence governs the evolution of immunological defence, but the costs and benefits specific to the adaptive immune system are poorly known. We used genetically engineered mice lacking lymphocytes (i.e. mice without adaptive, but with innate, immunity) as a model of the ancestral state in the evolution of the vertebrate immune system. To investigate if the magnitude of adaptive defence is constrained by the energetic costs of producing lymphocytes etc., we compared the basal metabolic rate of normal and lymphocyte-deficient mice. We found that lymphocyte-deficient mice had a higher basal metabolic rate than normal mice with both innate and adaptive immune defence. This suggests that the evolution of the adaptive immune system has not been constrained by energetic costs. Rather, it should have been favoured by the energy savings associated with a combination of innate and adaptive immune defence.

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Selected References

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  1. Agrawal A., Eastman Q. M., Schatz D. G. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature. 1998 Aug 20;394(6695):744–751. doi: 10.1038/29457. [DOI] [PubMed] [Google Scholar]
  2. Behnke J. M., Barnard C. J., Wakelin D. Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. Int J Parasitol. 1992 Nov;22(7):861–907. doi: 10.1016/0020-7519(92)90046-n. [DOI] [PubMed] [Google Scholar]
  3. Borghans J. A., Noest A. J., De Boer R. J. How specific should immunological memory be? J Immunol. 1999 Jul 15;163(2):569–575. [PubMed] [Google Scholar]
  4. Brown P. Cinderella goes to the ball. Nature. 2001 Apr 26;410(6832):1018–1020. doi: 10.1038/35074279. [DOI] [PubMed] [Google Scholar]
  5. Bründler M. A., Aichele P., Bachmann M., Kitamura D., Rajewsky K., Zinkernagel R. M. Immunity to viruses in B cell-deficient mice: influence of antibodies on virus persistence and on T cell memory. Eur J Immunol. 1996 Sep;26(9):2257–2262. doi: 10.1002/eji.1830260943. [DOI] [PubMed] [Google Scholar]
  6. Burnet F. M. Evolution of the immune process in vertebrates. Nature. 1968 May 4;218(5140):426–430. doi: 10.1038/218426a0. [DOI] [PubMed] [Google Scholar]
  7. Cheng S., Rothschild M. F., Lamont S. J. Estimates of quantitative genetic parameters of immunological traits in the chicken. Poult Sci. 1991 Oct;70(10):2023–2027. doi: 10.3382/ps.0702023. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Hill R. W. Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol. 1972 Aug;33(2):261–263. doi: 10.1152/jappl.1972.33.2.261. [DOI] [PubMed] [Google Scholar]
  11. Kaufmann S. H., Ladel C. H. Application of knockout mice to the experimental analysis of infections with bacteria and protozoa. Trends Microbiol. 1994 Jul;2(7):235–242. doi: 10.1016/0966-842x(94)90628-9. [DOI] [PubMed] [Google Scholar]
  12. Kitamura D., Roes J., Kühn R., Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 1991 Apr 4;350(6317):423–426. doi: 10.1038/350423a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Langhorne J., Mombaerts P., Tonegawa S. alpha beta and gamma delta T cells in the immune response to the erythrocytic stages of malaria in mice. Int Immunol. 1995 Jun;7(6):1005–1011. doi: 10.1093/intimm/7.6.1005. [DOI] [PubMed] [Google Scholar]
  15. Mombaerts P., Clarke A. R., Rudnicki M. A., Iacomini J., Itohara S., Lafaille J. J., Wang L., Ichikawa Y., Jaenisch R., Hooper M. L. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 1992 Nov 19;360(6401):225–231. doi: 10.1038/360225a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. doi: 10.1098/rspb.1999.0650. [DOI] [PMC free article] [Google Scholar]
  18. Read A. F., Allen J. E. Evolution and immunology. The economics of immunity. Science. 2000 Nov 10;290(5494):1104–1105. doi: 10.1126/science.290.5494.1104. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Segel L. A., Bar-Or R. L. On the role of feedback in promoting conflicting goals of the adaptive immune system. J Immunol. 1999 Aug 1;163(3):1342–1349. [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Smelt S. C., Cotterell S. E., Engwerda C. R., Kaye P. M. B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol. 2000 Apr 1;164(7):3681–3688. doi: 10.4049/jimmunol.164.7.3681. [DOI] [PubMed] [Google Scholar]
  24. Thompson C. B. New insights into V(D)J recombination and its role in the evolution of the immune system. Immunity. 1995 Nov;3(5):531–539. doi: 10.1016/1074-7613(95)90124-8. [DOI] [PubMed] [Google Scholar]

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