Abstract

Pathogen communities can vary substantially between geographical regions due to different environmental conditions. However, little is known about how host immune systems respond to environmental variation across macro-ecological and evolutionary scales. Here, we select 37 species of songbird that inhabit diverse environments, including African and Palaearctic residents and Afro-Palaearctic migrants, to address how climate and habitat have influenced the evolution of key immune genes, the major histocompatibility complex class I (MHC-I). Resident species living in wetter regions, especially in Africa, had higher MHC-I diversity than species living in drier regions, irrespective of the habitats they occupy. By contrast, no relationship was found between MHC-I diversity and precipitation in migrants. Our results suggest that the immune system of birds has evolved greater pathogen recognition in wetter tropical regions. Furthermore, evolving transcontinental migration appears to have enabled species to escape wet, pathogen-rich areas at key periods of the year, relaxing selection for diversity in immune genes and potentially reducing immune system costs.

Highlights

  • The adaptations that allow species to occupy different ecological niches have played a key role in shaping global patterns of biodiversity [1,2,3]

  • We investigated the relationship between major histocompatibility complex class I (MHC-I) diversity and the environments species inhabit using Bayesian phylogenetic mixed models (BPMM) implemented in the R package ‘MCMCglmm’ [47]

  • Despite the strong relationship between precipitation and the number of major histocompatibility complex (MHC)-I alleles, we found no significant association between MHC-I sequence divergence (P-distance) and precipitation in either the African or Palaearctic species

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Summary

Background

The adaptations that allow species to occupy different ecological niches have played a key role in shaping global patterns of biodiversity [1,2,3]. In order for an antigen to be determined as self or non-self, it must be presented to T cells by major histocompatibility complex (MHC) molecules, which are encoded by a set of highly polymorphic genes Diversity in these genes, both in terms of the number of unique alleles per individual and the sequence divergence in the peptide binding region (PBR) between alleles within individuals ( ‘MHC diversity’), increases the number of different antigenic peptides that can be bound and recognized by the immune system [24,25,26,27,28]. Passerida represent an ideal system for examining the effects of the environment on immunity as there are multiple evolutionary independent colonizations of different environments across the Palaearctic and Africa, as well as multiple origins of migration between these areas [31] Using this system, we have previously shown that yearround African residents have higher MHC-I diversity than Palaearctic residents and Afro-Palaearctic migrants [31]. We intersected species distribution maps with climatic databases and habitat information (proximity to water and lowland versus highland) to test the prediction that species living in wetter and warmer habitats 2 have higher MHC-I diversity than species living in drier and cooler habitats

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