Abstract
The Major Histocompatibility Complex (MHC) is a hyper-polymorphic genomic region, which forms a part of the vertebrate adaptive immune system and is crucial for intra- and extra-cellular pathogen recognition (MHC-I and MHC-IIA/B, respectively). Although recent advancements in high-throughput sequencing methods sparked research on the MHC in non-model species, the evolutionary history of MHC gene structure is still poorly understood in birds. Here, to explore macroevolutionary patterns in the avian MHC architecture, we retrieved contigs with antigen-presenting MHC and MHC-related genes from available genomes based on third-generation sequencing. We identified: 1) an ancestral avian MHC architecture with compact size and tight linkage between MHC-I, MHC-IIA/IIB and MHC-related genes; 2) three major patterns of MHC-IIA/IIB unit organization in different avian lineages; and 3) lineage-specific gene translocation events (e.g., separation of the antigen-processing TAP genes from the MHC-I region in passerines), and 4) the presence of a single MHC-IIA gene copy in most taxa, showing evidence of strong purifying selection (low dN/dS ratio and low number of positively selected sites). Our study reveals long-term macroevolutionary patterns in the avian MHC architecture and provides the first evidence of important transitions in the genomic arrangement of the MHC region over the last 100 million years of bird evolution.
Highlights
The major histocompatibility complex (MHC) is a central component of the vertebrate adaptive immune system, containing antigen-presenting class I (MHC-I) and class II (MHC-II) genes, which are primarily responsible for recognition of intra- and extra-cellular pathogens (Blum et al, 2013)
We searched for 10 genes of the MHC family across 45 TGSbased avian genomes and the number of retrieved gene copies varied between species (Tables 1, 2, Supplementary Tables S5, S6), this variation was unlikely to be driven by differences in genome quality
We found no significant association between the number of retrieved MHC-IIA and IIB copies (Spearman: R = 0.329, p = 0.062)
Summary
The major histocompatibility complex (MHC) is a central component of the vertebrate adaptive immune system, containing antigen-presenting class I (MHC-I) and class II (MHC-II) genes, which are primarily responsible for recognition of intra- and extra-cellular pathogens (Blum et al, 2013). Both MHC-I and MHC-II antigen-presenting molecules have a two-domain peptide-binding region (coded by exon 2 and 3 of a single MHC-I gene and by exon 2 of MHC-IIA and MHC-IIB genes), which directly bind to peptides. Gene arrangement, haplotype inference and linkage relationships at the avian MHC have all been clearly under-researched, mostly due to technical limitations (O’Connor et al, 2019)
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