Avian blood parasite richness decreases with major histocompatibility complex class I loci number

Abstract

Major histocompatibility complex (MHC) genes are among the most polymorphic in the vertebrate genome. The high allele diversity is believed to be maintained primarily by sexual and pathogen-mediated balancing selection. The number of MHC loci also varies greatly across vertebrates, most notably across birds. MHC proteins play key roles in presenting antigens on the cell surface for recognition by T cells, with class I proteins specifically targeting intracellular pathogens. Here, we explore the hypothesis that MHC class I diversity (measured as loci number) coevolves with haemosporidian parasite burden of the host. Using data on 54 bird species, we demonstrate that high-MHC class I diversity is associated with significantly lower richness of Plasmodium, Haemoproteus as well as overall haemosporidian parasite lineages, the former thus indicating more efficient protection against intracellular pathogens. Nonetheless, the latter associations were only detected when MHC diversity was assessed using cloning and not 454 pyrosequencing-based studies, nor across all genotyping methods combined. Our results indicate that high-MHC class I diversity might play a key role in providing qualitative resistance against diverse haemosporidian parasites in birds, but further clarification is needed for the origin of contrasting results when using different genotyping methods for MHC loci quantification.

Keywords: comparative analyses; copy number variation; haemosporidians; major histocompatibility complex diversity; parasite richness; pathogen-mediated selection.

Figure 1.

Association between residual blood parasite species richness and MHC-I diversity for (a) Plasmodium, (b) Haemoproteus, (c) Leucocytozoon and (d) overall haemosporidian lineages richness. Parasite diversity residuals were obtained from a log–log linear regressions between parasite lineages richness (dependent) and research effort (explanatory). Slopes were obtained from phylogenetic MCMCglmms with Poisson error distribution between parasite lineages richness and research effort as well as MHC-I diversity.