Abstract

BackgroundGenes of the Major Histocompatibility Complex (MHC) are essential for adaptive immune response in vertebrates, as they encode receptors that recognize peptides derived from the processing of intracellular (MHC class I) and extracellular (MHC class II) pathogens. High MHC diversity in natural populations is primarily generated and maintained by pathogen-mediated diversifying and balancing selection. It is, however, debated whether selection at the MHC can counterbalance the effects of drift in bottlenecked populations. The aim of this study was to assess allelic diversity of MHC genes in a recently bottlenecked bird of prey, the White-tailed Eagle Haliaeetus albicilla, as well as to compare mechanisms that shaped the evolution of MHC class I and class II in this species.ResultsWe showed that significant levels of MHC diversity were retained in the core Central European (Polish) population of White-tailed Eagles. Ten MHC class I and 17 MHC class II alleles were recovered in total and individual birds showed high average MHC diversity (3.80 and 6.48 MHC class I and class II alleles per individual, respectively). Distribution of alleles within individuals provided evidence for the presence of at least three class I and five class II loci the White-tailed Eagle, which suggests recent duplication events. MHC class II showed greater sequence polymorphism than MHC class I and there was much stronger signature of diversifying selection acting on MHC class II than class I. Phylogenetic analysis provided evidence for trans-species similarity of class II, but not class I, sequences, which is likely consistent with stronger balancing selection at MHC class II.ConclusionsRelatively high MHC diversity retained in the White-tailed Eagles from northern Poland reinforces high conservation value of local eagle populations. At the same time, our study is the first to demonstrate contrasting patterns of allelic diversity and selection at MHC class I and class II in an accipitrid species, supporting the hypothesis that different mechanisms can shape evolutionary trajectories of MHC class I and class II genes.

Highlights

  • Genes of the Major Histocompatibility Complex (MHC) are essential for adaptive immune response in vertebrates, as they encode receptors that recognize peptides derived from the processing of intracellular (MHC class I) and extracellular (MHC class II) pathogens

  • We found that White-tailed Eagle nestlings had lower allelic diversity at MHC class I than class II

  • We found evidence for much stronger positive selection acting on MHC class II than class I in the White-tailed Eagle

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Summary

Introduction

Genes of the Major Histocompatibility Complex (MHC) are essential for adaptive immune response in vertebrates, as they encode receptors that recognize peptides derived from the processing of intracellular (MHC class I) and extracellular (MHC class II) pathogens. Over 3500 MHC class I alleles were found within a Central European population of sedge warblers Acrocephalus schoenobaenus [7] and nearly a thousand MHC class II alleles were recorded in the common yellowthroat Geothlypis trichas [5]. This extreme MHC polymorphism is thought to be generated and maintained via pathogen-mediated diversifying and balancing selection [8], acting through the mechanisms of overdominance [9], negative frequency-dependence [10], and fluctuating selection [11]. Persistence of adaptive MHC alleles beyond species diversification due to balancing selection produces a pattern where some alleles are more similar between species than within species, which is referred to as trans-species polymorphism [12]

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