Abstract

The evolution and maintenance of conspicuous phenotypic polymorphisms has challenged evolutionary ecologists for centuries. Polymorphisms in pleiotropic cascades or genetic linkage may lead to correlations of life history traits such as immunity, parasite infection levels, pigmentation and lifetime reproductive success. The common buzzard Buteo buteo is a bird of prey occurring in several plumage morphs, which differ in pigmentation and in the prevalence, infection intensity and clone composition of their most common blood parasite, as well as in ectoparasite infestation levels. Buzzard morphs are heritable and exhibit a heterozygote advantage where intermediates have higher lifetime reproductive success (LRS). We explored the hypothesis that the differences in pigmentation also correspond to differences in immunity. We hence compared an inducible adaptive and an innate constitutive immune response between the buzzard plumage morphs. The increase of specific anti-tetanus antibodies after vaccination was explained by the morph of the nestling’s mother and was highest in offspring of intermediate mothers. Additionally, nestlings with higher humoral response were less infected with blood parasites and, if infected, harboured a lower genetic diversity of these parasites. The phytohaemagglutinin-induced skin swelling, a complex of cellular inflammatory responses, was lowest in intermediate nestlings. The higher LRS of intermediate buzzards suggests that the cellular immunity is an inferior fitness determinant compared to humoral immunity. The strength of immune responses was not linear along the melanisation gradient, indicating that there is most likely no simple genetic correlation between immune responses and plumage morphs.

Highlights

  • Understanding the mechanisms of polymorphism maintenance under selection continues to be a significant challenge for evolutionary biologists

  • The common buzzard Buteo buteo is a bird of prey occurring in several plumage morphs, which differ in pigmentation and in the prevalence, infection intensity and clone composition of their most common blood parasite, as well as in ectoparasite infestation levels

  • We showed that two components of the immune response are associated with plumage morphs of the common buzzard

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Summary

Introduction

Understanding the mechanisms of polymorphism maintenance under selection continues to be a significant challenge for evolutionary biologists. Melanin polymorphisms are widely distributed in many clades, but their adaptive significance still remains unclear (Fowlie and Kruger 2003; Roulin 2004). The pro-opiomelanocortin (POMC) pleiotropy has been suggested to cause positive correlations between pigmentation, humoral immunity and anti-inflammatory responses, since the involved hormones can regulate both the melanisation and systemic inflammation in mice (Ducrest et al 2008). Several studies have found correlations between melanin pigmentation and immune responses in wild vertebrates as a possible consequence of the POMC pleiotropy. The precise molecular link to the humoral response is so far unknown and the documented patterns are, at least partially, contradictory (Gangoso et al 2011, 2015; Jacquin et al 2011, 2013; Lei et al 2013; Roulin et al 2000)

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