Fitness Correlates of Heritable Variation in Antibody Responsiveness in a Wild Mammal

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Science  29 Oct 2010:
Vol. 330, Issue 6004, pp. 662-665
DOI: 10.1126/science.1194878

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Self-Recognition and Survival

Soay sheep are a remnant of an ancient breed of sheep that, although intensively studied for many years, live unmanaged on the remote Scottish island of St. Kilda. Life is harsh on the island, and the numbers of sheep show cycles of winter population crashes and high exposure to infection. Graham et al. (p. 662; see the Perspective by Martin and Coon) measured levels of self-reactive antibodies in the sheep called antinuclear antibodies (ANA). Having high ANA levels was a heritable trait that reflected generally high levels of immunoglobulin in individuals and of specific antibodies to parasitic worms. Female sheep with high levels of ANAs survived better during crash years, but had fewer births. If these sheep did reproduce, although the lambs tended to be small, they tended to have higher rates of early survival. Thus, maintaining high antibody levels apparently reflected investment in immunity and greater survival, but doing so was also associated with reduced reproductive success.


A functional immune system is important for survival in natural environments, where individuals are frequently exposed to parasites. Yet strong immune responses may have fitness costs if they deplete limited energetic resources or cause autoimmune disease. We have found associations between fitness and heritable self-reactive antibody responsiveness in a wild population of Soay sheep. The occurrence of self-reactive antibodies correlated with overall antibody responsiveness and was associated with reduced reproduction in adults of both sexes. However, in females, the presence of self-reactive antibodies was positively associated with adult survival during harsh winters. Our results highlight the complex effects of natural selection on immune responsiveness and suggest that fitness trade-offs may maintain immunoheterogeneity, including genetic variation in autoimmune susceptibility.

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