Natural Selection on Antihelminth Antibodies in a Wild Mammal Population

Abstract

An effective immune response is expected to confer fitness benefits through improved resistance to parasites but also incur energetic costs that 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 26 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 antiparasite IgA best predicted reduced egg counts, but this did not predict survival in lambs. In adults increased antiparasite IgG predicted reduced egg counts, and in adult females IgG levels also positively predicted overwinter 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 among functionally related immune markers.

The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries)

“…parasitic helminth antigens) and produced by the same arm of the immune system, genetic correlations among measures can still be weak. Our findings also highlight the importance of age-dependence in the genetic control of immune phenotypes, mirroring our recent finding that selection on these three isotypes is highly age-dependent in this study system [60]. Whilst the inter-isotype genetic correlations were highly positive in lambs (r A ≥ 0.695), they were much smaller in adults (r A ≤ 0.232).…”

“…It is notable that adult IgG, as well as being under the strongest directional selection, also has the lowest heritability compared to other isotypes and age groups (Fig 2, Table 1). This is consistent with the prediction that directional selection should erode heritable variation, whilst the high observed heritabilities in general are consistent with observations of weak or variable selection on these antibody measures [60]. Nevertheless, a full understanding of the mechanisms maintaining this genetic variation will require examination of association between genotypes at significant loci with individual fitness, i.e.…”

“…Alternatively, the observed high heritabilities in both domestic and wild sheep may be in accordance with theory predicting that stabilising selection, rather than directional selection, is likely to be acting on immune traits [75], which in turn may lead to the maintenance of genetic variation at the underlying trait loci. In the Soay sheep, we have shown with the same dataset that there is little evidence for stabilising selection, with directional selection present for IgG in adults but not for other isotypes or age groups [60]. It is notable that adult IgG, as well as being under the strongest directional selection, also has the lowest heritability compared to other isotypes and age groups (Fig 2, Table 1).…”

“…Parasite-specific antibody responses are moderately heritable [28,57] and parasite-specific IgA levels and parasite-specific pan-isotype antibody levels have been shown to be negatively associated with strongyle faecal egg count [26,57]. Recent examination of anti-nematode antibody isotypes (namely IgA, IgE and IgG) over a 26-year period showed that levels of IgG are positively associated with adult survival, and negative associations are observed between antibodies and FEC for all isotypes in lambs, but only for IgG in adults [58–60].…”

The demographic pattern of infection with chronic wasting disease in reindeer at an early epidemic stage

“…A common pattern among mammals is higher infection levels in males compared to females (Schalk and Forbes 1997, C ordoba-Aguilar and Mungu ıa-Steyer 2013, Metcalf and Graham 2018 and in the young and senescent compared to prime-aged individuals (Hayward et al 2011, Abolins et al 2018, Benton et al 2018. However, there are many exceptions to these main demographic infection patterns (Vicente et al 2007, Smyth and Drea 2016, Sparks et al 2018. Differences in behavior and contact rates affect the likelihood of pathogen exposure, and such variability differs predictably between sexes and age classes (Smyth andDrea 2016, Silk et al 2018).…”