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Expansion of MHC-IIB Has Constrained the Evolution of MHC-IIA in Passerines

Ruesink-Bueno, Iris Liesbeth LU ; Drews, Anna LU ; O’Connor, Emily Amelia LU orcid and Westerdahl, Helena LU (2024) In Genome Biology and Evolution 16(11).
Abstract

The major histocompatibility complex (MHC) is central in adaptive immunity, with the highly polymorphic MHC genes encoding antigen-presenting molecules. Two MHC class II (MHC-II) loci, DA1 and DA2, predate the radiation of extant birds and persist throughout much of the avian phylogeny. Within each locus, the MHC-II molecules are encoded by A-genes (DAA) and B-genes (DAB), which are arranged in A–B dyads. However, in passerines (order Passeriformes), the DA2 locus has been lost, and the ancestral A–B dyad at the DA1 locus has been replaced by a putatively single A-gene (DAA1) and an array of highly polymorphic B-genes (DAB1). In this study, we genotyped the DAA1 gene of 15 passerine species and confirmed that passerines possess just one... (More)

The major histocompatibility complex (MHC) is central in adaptive immunity, with the highly polymorphic MHC genes encoding antigen-presenting molecules. Two MHC class II (MHC-II) loci, DA1 and DA2, predate the radiation of extant birds and persist throughout much of the avian phylogeny. Within each locus, the MHC-II molecules are encoded by A-genes (DAA) and B-genes (DAB), which are arranged in A–B dyads. However, in passerines (order Passeriformes), the DA2 locus has been lost, and the ancestral A–B dyad at the DA1 locus has been replaced by a putatively single A-gene (DAA1) and an array of highly polymorphic B-genes (DAB1). In this study, we genotyped the DAA1 gene of 15 passerine species and confirmed that passerines possess just one copy of DAA1. We then compared selection patterns in DAA1 between passerines and nonpasserines and found that exon 2, which encodes the antigen-presenting domain, has been subject to weaker positive selection and stronger negative selection in passerines compared with nonpasserines. Additional comparisons showed that the patterns of selection in the passerine DAA1 gene are unlikely to be related to the loss of the DA2 locus. Instead, our findings suggest that the expansion of DAB1 (MHC-IIB) has imposed an evolutionary constraint on the passerine DAA1 (MHC-IIA) gene. We speculate that this constraint may be the result of each DAA1 chain forming heterodimers with many different DAB1 chains.

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author
; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
macroevolution, major histocompatibility complex (MHC), MHC-IIA, negative selection, Passeriformes, positive selection
in
Genome Biology and Evolution
volume
16
issue
11
article number
evae236
publisher
Oxford University Press
external identifiers
  • pmid:39462092
  • scopus:85209479318
ISSN
1759-6653
DOI
10.1093/gbe/evae236
language
English
LU publication?
yes
additional info
Publisher Copyright: © The Author(s) 2024.
id
ef119733-0248-4d2d-9291-bc92510c3f45
date added to LUP
2025-01-13 17:18:28
date last changed
2025-07-01 07:18:40
@article{ef119733-0248-4d2d-9291-bc92510c3f45,
  abstract     = {{<p>The major histocompatibility complex (MHC) is central in adaptive immunity, with the highly polymorphic MHC genes encoding antigen-presenting molecules. Two MHC class II (MHC-II) loci, DA1 and DA2, predate the radiation of extant birds and persist throughout much of the avian phylogeny. Within each locus, the MHC-II molecules are encoded by A-genes (DAA) and B-genes (DAB), which are arranged in A–B dyads. However, in passerines (order Passeriformes), the DA2 locus has been lost, and the ancestral A–B dyad at the DA1 locus has been replaced by a putatively single A-gene (DAA1) and an array of highly polymorphic B-genes (DAB1). In this study, we genotyped the DAA1 gene of 15 passerine species and confirmed that passerines possess just one copy of DAA1. We then compared selection patterns in DAA1 between passerines and nonpasserines and found that exon 2, which encodes the antigen-presenting domain, has been subject to weaker positive selection and stronger negative selection in passerines compared with nonpasserines. Additional comparisons showed that the patterns of selection in the passerine DAA1 gene are unlikely to be related to the loss of the DA2 locus. Instead, our findings suggest that the expansion of DAB1 (MHC-IIB) has imposed an evolutionary constraint on the passerine DAA1 (MHC-IIA) gene. We speculate that this constraint may be the result of each DAA1 chain forming heterodimers with many different DAB1 chains.</p>}},
  author       = {{Ruesink-Bueno, Iris Liesbeth and Drews, Anna and O’Connor, Emily Amelia and Westerdahl, Helena}},
  issn         = {{1759-6653}},
  keywords     = {{macroevolution; major histocompatibility complex (MHC); MHC-IIA; negative selection; Passeriformes; positive selection}},
  language     = {{eng}},
  month        = {{11}},
  number       = {{11}},
  publisher    = {{Oxford University Press}},
  series       = {{Genome Biology and Evolution}},
  title        = {{Expansion of MHC-IIB Has Constrained the Evolution of MHC-IIA in Passerines}},
  url          = {{http://dx.doi.org/10.1093/gbe/evae236}},
  doi          = {{10.1093/gbe/evae236}},
  volume       = {{16}},
  year         = {{2024}},
}