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Extreme MHC class i diversity in the sedge warbler (Acrocephalus schoenobaenus); Selection patterns and allelic divergence suggest that different genes have different functions

Biedrzycka, Aleksandra; O'Connor, Emily LU ; Sebastian, Alvaro; Migalska, Magdalena; Radwan, Jacek; Zając, Tadeusz; Bielański, Wojciech; Solarz, Wojciech; Ćmiel, Adam and Westerdahl, Helena LU (2017) In BMC Evolutionary Biology 17(1).
Abstract

Background: Recent 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... (More)

Background: Recent 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. Results: The 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. Conclusions: Our 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.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Different functions of loci, Extreme diversity, MHC class I, Sedge warbler
in
BMC Evolutionary Biology
volume
17
issue
1
publisher
BioMed Central
external identifiers
  • scopus:85021264457
  • wos:000404927000001
ISSN
1471-2148
DOI
10.1186/s12862-017-0997-9
language
English
LU publication?
yes
id
87fa543c-daf4-4eb4-8133-33ce9386b9f3
date added to LUP
2017-07-26 10:34:33
date last changed
2018-07-08 04:25:52
@article{87fa543c-daf4-4eb4-8133-33ce9386b9f3,
  abstract     = {<p>Background: Recent 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. Results: The 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. Conclusions: Our 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.</p>},
  articleno    = {159},
  author       = {Biedrzycka, Aleksandra and O'Connor, Emily and Sebastian, Alvaro and Migalska, Magdalena and Radwan, Jacek and Zając, Tadeusz and Bielański, Wojciech and Solarz, Wojciech and Ćmiel, Adam and Westerdahl, Helena},
  issn         = {1471-2148},
  keyword      = {Different functions of loci,Extreme diversity,MHC class I,Sedge warbler},
  language     = {eng},
  month        = {07},
  number       = {1},
  publisher    = {BioMed Central},
  series       = {BMC Evolutionary Biology},
  title        = {Extreme MHC class i diversity in the sedge warbler (Acrocephalus schoenobaenus); Selection patterns and allelic divergence suggest that different genes have different functions},
  url          = {http://dx.doi.org/10.1186/s12862-017-0997-9},
  volume       = {17},
  year         = {2017},
}