“Natural selection on anti-helminth antibodies in a wild mammal population”

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Alexandra M. Sparks, Kathryn Watt, Rona Sinclair, Jill G. Pilkington, Josephine M. Pemberton, Susan E. Johnston, Tom N. McNeilly, and Daniel H. Nussey (Dec 2018)

The DOI will be https://dx.doi.org/10.1086/700115

Natural selection on immune responses vary across demographic groups but not environments in a wild mammal population

A view of the study area at Village Bay on the island of Hirta in the St Kilda archipelago.
(Photo © Alexandra M. Sparks)

The immune system is crucial in defending individuals against a multitude of parasites, and consequently effective immune responses are expected to be under selection. However, studies in the wild have shown there is considerable variation in immune responses between individuals. One explanation for the maintenance of such variability is that immune responses are energetically costly and this results in trade-offs with other traits such as growth and reproduction. The costs and benefits of immune responses may also vary by age and sex of the individual as well as their environment, but few studies have investigated this.

A Soay ewe.
(Photo © Kara Dicks)

Using data from a long-term individual-based study of wild Soay sheep living unmanaged in the St Kilda archipelago, the authors measured anti-parasite antibodies (IgA, IgE, IgG) in blood samples collected from sheep caught over a 25-year period. They then investigated whether these antibodies were associated with parasite fecal egg counts (a measure of parasite burden), weight, over-winter survival, and breeding success. Contrary to predictions, they did not find strong evidence for environment-dependent selection or costs associated with reproduction. The authors did find that high antibody levels predicted lower parasite egg counts and over-winter survival; however, this was dependent on the antibody isotype as well as the age and sex of the individual. Lambs with higher IgA levels had lower parasite egg counts but none of the antibodies were associated with over-winter survival. In contrast, adults with higher IgG levels had lower parasite egg counts and adult females with higher IgG levels were more likely to survive over winter. These results highlight the complexity of natural selection on immune traits in the wild and suggest that patterns of selection are unlikely to generalize across different immune measures or host demographic groups.


Abstract

An effective immune response is expected to confer fitness benefits through improved resistance to parasites but also incur energetic costs which negatively impact fitness-related traits such as reproduction. The fitness costs and benefits of an immune response are likely to depend on host age, sex, and levels of parasite exposure. Few studies have examined the full extent to which patterns of natural selection on immune phenotypes vary across demographic groups and environments in the wild. Here, we assessed natural selection on plasma levels of three functionally distinct isotypes (IgA, IgE and IgG) of antibodies against a prevalent nematode parasite measured in a wild Soay sheep population over 25 years. We found little support for environment-dependent selection or reproductive costs. However, antibody levels were negatively associated with parasite egg counts and positively associated with subsequent survival, albeit in a highly age- and isotype-dependent manner. Raised levels of anti-parasite IgA best predicted reduced egg counts but this did not predict survival in lambs. In adults increased anti-parasite IgG predicted reduced egg counts and in adult females IgG levels also positively predicted over-winter survival. Our results highlight the potential importance of age- and sex-dependent selection on immune phenotypes in nature, and show that patterns of selection can vary even amongst functionally-related immune markers.