Abstract
BackgroundRecent work suggests that gene duplications may play an important role in the evolution of immunity genes. Passerine birds, and in particular Sylvioidea warblers, have highly duplicated major histocompatibility complex (MHC) genes, which are key in immunity, compared to other vertebrates. However, reasons for this high MHC gene copy number are yet unclear. High-throughput sequencing (HTS) allows MHC genotyping even in individuals with extremely duplicated genes. This HTS data can reveal evidence of selection, which may help to unravel the putative functions of different gene copies, i.e. neofunctionalization. We performed exhaustive genotyping of MHC class I in a Sylvioidea warbler, the sedge warbler, Acrocephalus schoenobaenus, using the Illumina MiSeq technique on individuals from a wild study population.ResultsThe MHC diversity in 863 genotyped individuals by far exceeds that of any other bird species described to date. A single individual could carry up to 65 different alleles, a large proportion of which are expressed (transcribed). The MHC alleles were of three different lengths differing in evidence of selection, diversity and divergence within our study population. Alleles without any deletions and alleles containing a 6 bp deletion showed characteristics of classical MHC genes, with evidence of multiple sites subject to positive selection and high sequence divergence. In contrast, alleles containing a 3 bp deletion had no sites subject to positive selection and had low divergence.ConclusionsOur results suggest that sedge warbler MHC alleles that either have no deletion, or contain a 6 bp deletion, encode classical antigen presenting MHC molecules. In contrast, MHC alleles containing a 3 bp deletion may encode molecules with a different function. This study demonstrates that highly duplicated MHC genes can be characterised with HTS and that selection patterns can be useful for revealing neofunctionalization. Importantly, our results highlight the need to consider the putative function of different MHC genes in future studies of MHC in relation to disease resistance and fitness.
Highlights
Recent work suggests that gene duplications may play an important role in the evolution of immunity genes
Long cDNA reads from Sanger sequencing We obtained 12 verified 729-735 bp major histocompatibility complex (MHC) class I transcripts from two sedge warbler individuals
The sedge warbler cDNAs were aligned to previously published MHC class I transcripts from other songbirds and many conserved sites were verified (e.g. cysteines (C) at positions 99, 163 and 201, sites known to bind the C- and N-terminal of peptides at positions 58Y, 141 T, 145 W, 158Y and 170Y, and the CD8 binding sites at positions 220–244)
Summary
Recent work suggests that gene duplications may play an important role in the evolution of immunity genes. In particular Sylvioidea warblers, have highly duplicated major histocompatibility complex (MHC) genes, which are key in immunity, compared to other vertebrates. Reasons for this high MHC gene copy number are yet unclear. High-throughput sequencing (HTS) allows MHC genotyping even in individuals with extremely duplicated genes This HTS data can reveal evidence of selection, which may help to unravel the putative functions of different gene copies, i.e. neofunctionalization. Classical MHC genes encode molecules of central importance in vertebrate adaptive immunity [12]. These MHC molecules are responsible for presenting antigens (peptides) to the immune system for recognition and elimination [13]. There is a group of MHC genes that have limited expression, low polymorphism and a less clear role in immunity, and these genes are referred to as non-classical MHC genes [26]
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