MHC polymorphism in a songbird: Fitness, mate choice, and sexual conflict

Research output: ThesisDoctoral Thesis (compilation)

Abstract

Sex differences in immune responses have been observed across a wide range of animal species, with the general
tendency that males have weaker immune responses than females. These differences are at least partly caused by immune-regulating effects of sex hormones, and have been associated with an increased prevalence of autoimmune disorders in females and with a general tendency for males to be parasitized more often than females. Because of these differences, male and female phenotypes may be regarded as different immunological environments, however it has not previously been investigated whether sex differences in immune responses may lead to sexually antagonistic selection on immune system genes.
The first chapter of this thesis presents a literature study of the effects of sex hormones on the strength of immune responses in vertebrates, based on which we propose the hypothesis that sexual selection may drive sexually antagonistic selection on genes associated with the immune system. In the following chapters, we investigated this hypothesis using major histocompatibility complex class I (MHC-I) genes in a species subject to strong sexual selection, a socially polygynous songbird, the great reed warbler Acrocephalus arundinaceus.
MHC genes play an important role in vertebrate adaptive immunity where they enable recognition and elimination of pathogens. Due to an ongoing co-evolution between hosts and their pathogens, the MHC genes are among the most variable genes known in vertebrates. It has been hypothesized that hosts benefit from having high MHC diversity, because this confers protection against a wider range of pathogens. Interestingly, we found evidence for a sexual conflict and for sexually differential selection on MHC-I diversity in our great reed warbler study population.
It has been predicted that genes associated with disease resistance should be advantageous in terms of sexual selection, and this prediction is central to our hypothesis that sexual selection may drive sexually antagonistic selection on genes associated with the immune system. We therefore investigated whether MHC-I genes were associated with sexual selection in great reed warblers. Our results indicated that MHC-I diversity (i) conveys a ‘good genes’ benefit to females that select older males and males with large song repertoires, and (ii) affects the ability of males to acquire attractive territories. These results confirmed that MHC-I genes are associated with sexual selection, and thereby corroborated our hypothesis that sexual selection may be driving the observed sexual conflict over MHC-I diversity via immune regulating effects of sex hormones.
Finally, we investigated the source of MHC-I genotypic variation in great reed warblers by analyzing segregation of MHC-I haplotypes and performing phylogenetic reconstruction on MHC-I alleles. We identified five distinct clades in a phylogenetic tree that indicate the presence of several divergent MHC-I loci in the great reed warbler genome. Analyses of positive selection implied that each putative MHC-I locus may have evolved slightly different functions. Importantly, variation in MHC-I diversity between haplotypes was largely explained by variation within two specific clades, suggesting that the sexual conflict over MHC-I diversity may be caused by sexually antagonistic effects associated with alleles from these clades in particular.
Our results suggest that sexually antagonistic selection is an important force in the evolution of vertebrate adaptive immunity, which may be important for a comprehensive, evolutionary understanding of autoimmune diseases and other costs associated with immune responses in vertebrates. The results presented in this thesis invite further studies that investigate the generality of sexually antagonistic selection over immune system genes in other species, as well as more detailed studies of the mechanisms underlying such sexual conflicts.

Details

Authors
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Research areas and keywords

Subject classification (UKÄ) – MANDATORY

  • Evolutionary Biology
  • Ecology
  • Immunology

Keywords

  • Major histocompatibility complex, MHC diversity, MHC haplotypes, sexually antagonistic selection, costs of immune responses, adaptive immunity, great reed warbler, songbird
Original languageEnglish
QualificationDoctor
Awarding Institution
Supervisors/Assistant supervisor
Award date2019 Feb 15
Place of PublicationLund
Publisher
  • Biologiska institutionen, Lunds universitet
Print ISBNs978-91-7753-929-2
Electronic ISBNs978-91-7753-930-8
Publication statusPublished - 2019 Jan
Publication categoryResearch

Bibliographic note

Defence details Date: 2019-02-15 Time: 13:30 Place: The Blue Hall, the Ecology Building, Sölvegatan 37, Lund External reviewer(s) Name: Piertney, Stuart Title: Professor Affiliation: University of Aberdeen, UK ---

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