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.
Highlights
Parasites have a major impact on host condition and fitness and thereby represent a strong selective force for individuals in natural populations (Schmid-Hempel 2011)
In a model containing all three antibody isotypes, isotypes and annual breeding probability (IgA) levels were independently negatively associated with fecal egg count (FEC) (b p 20:074 5 0:021 standard errors (SEs), x2(1) p 11:860, P p :001), while IgE and IgG were no longer significantly associated with FEC (IgE: b p 20:030 5 0:020 SE, x2(1) p 2:180, P p :140; IgG: b p 20:034 5 0:022 SE, x2(1) p 2:420, P p :120)
We found no evidence for sex- or density-dependent effects of antibody levels on FEC in lambs
Summary
Parasites have a major impact on host condition and fitness and thereby represent a strong selective force for individuals in natural populations (Schmid-Hempel 2011). The main defense against parasites is the host immune system (Murphy 2012), and it is expected for there to be a strong directional selection in favor of robust and effective immune responses in natural populations (Nunn et al 2000; Lindström et al 2004; Scharsack et al 2007). Mounting strong immune responses can lead to damage to host tissue and autoimmunity, which would impose a fitness cost (Graham et al 2005; Viney et al 2005). These processes could result in a pattern of stabilizing—rather than directional selection—on immune phenotypes (Seppälä 2015)
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