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. 2003 Oct 22;270(1529):2151–2157. doi: 10.1098/rspb.2003.2480

Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects.

Jane M Reid 1, Peter Arcese 1, Lukas F Keller 1
PMCID: PMC1691491  PMID: 14561279

Abstract

A thorough knowledge of relationships between host genotype and immunity to parasitic infection is required to understand parasite-mediated mechanisms of genetic and population change. It has been suggested that immunity may decline with inbreeding. However, the relationship between inbreeding level and a host's response to a novel immune challenge has not been investigated in a natural population. We used the pedigreed population of song sparrows (Melospiza melodia) inhabiting Mandarte Island, Canada, to test the hypothesis that a sparrow's cell-mediated immune response (CMI) to an experimental challenge would decline with individual or parental inbreeding. CMI in 6-day-old chicks declined significantly with their mother's coefficient of inbreeding, demonstrating an inter-generational effect of maternal inbreeding on offspring immunity. In fledged juveniles and adult sparrows, CMI declined markedly with an individual's own coefficient of inbreeding, but not its mother's. This relationship was consistent across seasons, and was not attributable solely to heterosis in offspring of immigrant breeders. CMI also declined with age and increased with body condition in adult sparrows, but inbreeding explained 37% of the total variation. We emphasize the implications of this dramatic inbreeding depression in cell-mediated immunity for theories of parasite-mediated evolution and the susceptibility of small, inbred populations.

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Selected References

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  1. Carrington M., Nelson G. W., Martin M. P., Kissner T., Vlahov D., Goedert J. J., Kaslow R., Buchbinder S., Hoots K., O'Brien S. J. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science. 1999 Mar 12;283(5408):1748–1752. doi: 10.1126/science.283.5408.1748. [DOI] [PubMed] [Google Scholar]
  2. Cheng S., Lamont S. J. Genetic analysis of immunocompetence measures in a White Leghorn chicken line. Poult Sci. 1988 Jul;67(7):989–995. doi: 10.3382/ps.0670989. [DOI] [PubMed] [Google Scholar]
  3. Christe P., Moller A. P., Saino N., De Lope F. Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity (Edinb) 2000 Jul;85(Pt 1):75–83. doi: 10.1046/j.1365-2540.2000.00732.x. [DOI] [PubMed] [Google Scholar]
  4. Desjardins P. J., Norris L. H., Cooper S. A., Reynolds D. C. Analgesic efficacy of intranasal butorphanol (Stadol NS) in the treatment of pain after dental impaction surgery. J Oral Maxillofac Surg. 2000 Oct;58(10 Suppl 2):19–26. doi: 10.1053/joms.2000.17884. [DOI] [PubMed] [Google Scholar]
  5. Duffy Deborah L., Ball Gregory F. Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc Biol Sci. 2002 Apr 22;269(1493):847–852. doi: 10.1098/rspb.2002.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ferguson M. M., Drahushchak L. R. Disease resistance and enzyme heterozygosity in rainbow trout. Heredity (Edinb) 1990 Jun;64(Pt 3):413–417. doi: 10.1038/hdy.1990.52. [DOI] [PubMed] [Google Scholar]
  7. Gasparini J., McCoy K. D., Haussy C., Tveraa T., Boulinier T. Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc Biol Sci. 2001 Mar 22;268(1467):647–650. doi: 10.1098/rspb.2000.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goto N., Kodama H., Okada K., Fujimoto Y. Suppression of phytohemagglutinin skin response in thymectomized chickens. Poult Sci. 1978 Jan;57(1):246–250. doi: 10.3382/ps.0570246. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Keller L. F., Jeffery K. J., Arcese P., Beaumont M. A., Hochachka W. M., Smith J. N., Bruford M. W. Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc Biol Sci. 2001 Jul 7;268(1474):1387–1394. doi: 10.1098/rspb.2001.1607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lozano George A., Lank David B. Seasonal trade-offs in cell-mediated immunosenescence in ruffs (Philomachus pugnax). Proc Biol Sci. 2003 Jun 7;270(1520):1203–1208. doi: 10.1098/rspb.2002.2309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Marr Amy B., Keller Lukas F., Arcese Peter. Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution. 2002 Jan;56(1):131–142. doi: 10.1111/j.0014-3820.2002.tb00855.x. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. doi: 10.1098/rspb.1997.0141. [DOI] [PMC free article] [Google Scholar]
  15. doi: 10.1098/rspb.1997.0222. [DOI] [PMC free article] [Google Scholar]
  16. doi: 10.1098/rspb.1998.0432. [DOI] [PMC free article] [Google Scholar]
  17. doi: 10.1098/rspb.1998.0481. [DOI] [PMC free article] [Google Scholar]
  18. doi: 10.1098/rspb.1999.0925. [DOI] [PMC free article] [Google Scholar]
  19. Paterson S., Wilson K., Pemberton J. M. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3714–3719. doi: 10.1073/pnas.95.7.3714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Smith J. A., Wilson K., Pilkington J. G., Pemberton J. M. Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proc Biol Sci. 1999 Jun 22;266(1425):1283–1290. doi: 10.1098/rspb.1999.0776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Taylor R. L., Jr, Cotter P. F., Wing T. L., Briles W. E. Major histocompatibility (B) complex and sex effects on the phytohaemagglutinin wattle response. Anim Genet. 1987;18(4):343–350. doi: 10.1111/j.1365-2052.1987.tb00778.x. [DOI] [PubMed] [Google Scholar]
  23. Warner C. M., Meeker D. L., Rothschild M. F. Genetic control of immune responsiveness: a review of its use as a tool for selection for disease resistance. J Anim Sci. 1987 Feb;64(2):394–406. doi: 10.2527/jas1987.642394x. [DOI] [PubMed] [Google Scholar]

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