Divergence between genes but limited allelic polymorphism in two MHC class II A genes in Leach’s storm-petrels Oceanodroma leucorhoa

Rand, Laura M.; Woodward, Carla; May, Rose; Ackerman, Ross; Tweedie, Bridget; Zicarelli, T. Bruno; Dearborn, Donald C.

doi:10.1007/s00251-019-01130-z

Cited by 4 publications

(6 citation statements)

References 59 publications

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“…Therefore, our finding of one to at least three gene copies of both MHC classes in common buzzards from multiple forms of high-throughput sequencing data was unexpected, and strongly suggests CNV is present in this species. We also found tandem pairs of class IIA and IIB genes in our long-read data, consistent with tandem duplications seen in mammals [ 64 ] and in some non-model bird species [ 65 – 67 ]. By retrieving sequences from haplotype-aware contig long-read assemblies and blast-searching them against RNAseq transcripts, we were able to confirm that all three loci for each MHC class are expressed (Additional file Table S 4 ).…”

Section: Discussionsupporting

confidence: 89%

High functional allelic diversity and copy number in both MHC classes in the common buzzard

et al. 2023

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Background The major histocompatibility complex (MHC), which encodes molecules that recognize various pathogens and parasites and initiates the adaptive immune response in vertebrates, is renowned for its exceptional polymorphism and is a model of adaptive gene evolution. In birds, the number of MHC genes and sequence diversity varies greatly among taxa, believed due to evolutionary history and differential selection pressures. Earlier characterization studies and recent comparative studies suggest that non-passerine species have relatively few MHC gene copies compared to passerines. Additionally, comparative studies that have looked at partial MHC sequences have speculated that non-passerines have opposite patterns of selection on MHC class I (MHC-I) and class II (MHC-II) loci than passerines: namely, greater sequence diversity and signals of selection on MHC-II than MHC-I. However, new sequencing technology is revealing much greater MHC variation than previously expected while also facilitating full sequence variant detection directly from genomic data. Our study aims to take advantage of high-throughput sequencing methods to fully characterize both classes and domains of MHC of a non-passerine bird of prey, the common buzzard (Buteo buteo), to test predictions of MHC variation and differential selection on MHC classes. Results Using genetic, genomic, and transcriptomic high-throughput sequencing data, we established common buzzards have at least three loci that produce functional alleles at both MHC classes. In total, we characterize 91 alleles from 113 common buzzard chicks for MHC-I exon 3 and 41 alleles from 125 chicks for MHC-IIB exon 2. Among these alleles, we found greater sequence polymorphism and stronger diversifying selection at MHC-IIB exon 2 than MHC-I exon 3, suggesting differential selection pressures on MHC classes. However, upon further investigation of the entire peptide-binding groove by including genomic data from MHC-I exon 2 and MHC-IIA exon 2, this turned out to be false. MHC-I exon 2 was as polymorphic as MHC-IIB exon 2 and MHC-IIA exon 2 was essentially invariant. Thus, comparisons between MHC-I and MHC-II that included both domains of the peptide-binding groove showed no differences in polymorphism nor diversifying selection between the classes. Nevertheless, selection analysis indicates balancing selection has been acting on common buzzard MHC and phylogenetic inference revealed that trans-species polymorphism is present between common buzzards and species separated for over 33 million years for class I and class II. Conclusions We characterize and confirm the functionality of unexpectedly high copy number and allelic diversity in both MHC classes of a bird of prey. While balancing selection is acting on both classes, there is no evidence of differential selection pressure on MHC classes in common buzzards and this result may hold more generally once more data for understudied MHC exons becomes available.

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Section: Discussionsupporting

confidence: 89%

High functional allelic diversity and copy number in both MHC classes in the common buzzard

et al. 2023

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“…Nevertheless, we are aware of only two population-wide screening studies of MHC-IIA genes in birds (chicken and the Leach’s storm-petrel Oceanodroma leucorhoa ), and both showed a low level of polymorphism. Specifically, there were only four nucleotide and one amino acid polymorphisms detected within a single MHC-IIA gene in the chicken ( Salomonsen et al, 2003 ), whereas two IIA genes were found in the storm-petrel: DAA with a single allele and DBA with three alleles differing from each other by single non-synonymous substitutions ( Rand et al, 2019 ). This clearly contrasted with markedly diverged MHC-IIB alleles, as found in the same study ( Rand et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, there were only four nucleotide and one amino acid polymorphisms detected within a single MHC-IIA gene in the chicken ( Salomonsen et al, 2003 ), whereas two IIA genes were found in the storm-petrel: DAA with a single allele and DBA with three alleles differing from each other by single non-synonymous substitutions ( Rand et al, 2019 ). This clearly contrasted with markedly diverged MHC-IIB alleles, as found in the same study ( Rand et al, 2019 ). Here, we only examined MHC-IIA sequences from one individual per species, so we had no insight into the intra-specific MHC-IIA variation and we can only discuss polymorphism across species.…”

Section: Discussionmentioning

confidence: 99%

Reconstructing Macroevolutionary Patterns in Avian MHC Architecture With Genomic Data

He¹,

Liang²,

Zhu

et al. 2022

Front. Genet.

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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.

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“…Although we acknowledge that the hypothesis on the specialization of gene lineages in terms of antigen recognition is highly speculative, we recommend that it should be put to further investigation at the intra-specific level. So far, we are aware of intra-specific comparisons of selection at both gene lineages only in a single bird species, clearly showing sequence divergence and codon-specific differences in selection signal between the peptide-binding domains of the two gene lineages in the Leach’s storm petrel ( 57 , 58 ). Interestingly, MHC-IIB sequences showed much greater sequence divergence between gene lineages than MHC-IIA and this divergence was found to be primarily driven by positive selection concentrating at the putative peptide-binding sites, suggesting possible functional differences in antigen recognition ( 58 ).…”

Section: Discussionmentioning

confidence: 99%

Ancient duplication, coevolution, and selection at the MHC class IIA and IIB genes of birds

Minias,

Edwards,

Babik

2023

Front. Immunol.

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IntroductionThe Major Histocompatibility Complex (MHC) of vertebrates is a dynamically evolving multigene family primarily responsible for recognizing non-self peptide antigens and triggering a pathogen-specific adaptive immune response. In birds, the MHC was previously thought to evolve via concerted evolution with high degree of gene homogenization and the rapid loss of orthology. However, the discovery of two ancient avian MHC-IIB gene lineages (DAB1 and DAB2) originating before the radiation of extant birds indicated that despite the action of concerted evolution, orthology may be detectable for long evolutionary periods.MethodsHere, we take advantage of rapidly accumulating digital genomic resources to search for the signal of an ancient duplication at the avian MHC-IIA genes, as well as to compare phylogenetic distribution and selection between MHC-IIA and IIB gene lineages.ResultsThe analysis of MHC sequences from over 230 species representing ca. 70 bird families revealed the presence of two ancient MHC-IIA gene lineages (DAA1 and DAA2) and showed that their phylogenetic distribution matches exactly the distribution of DAB1 and DAB2 lineages, suggesting tight coevolution. The early post-duplication divergence of DAA1 and DAA2 was driven by positive selection fixing radical amino acid differences within the membrane-proximal domain and, most probably, being functionally related to the interactions between α2 and β2 chains of the MHC-II heterodimer. We detected no evidence for an overall (gene-wide) relaxation or intensification of selection at either DAA1/DAB1 or DAA2/DAB2, but codon-specific differences in selection signature were found at the peptide-binding sites between the two gene lineages, perhaps implying specialization to different pathogen regimes.DiscussionOur results suggest that specific pairing of MHC-II α and β chains may have an adaptive significance, a conclusion that advances knowledge on the macroevolution of the avian MHC-II and opens exciting novel directions for future research.

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Divergence between genes but limited allelic polymorphism in two MHC class II A genes in Leach’s storm-petrels Oceanodroma leucorhoa

Cited by 4 publications

References 59 publications

High functional allelic diversity and copy number in both MHC classes in the common buzzard

High functional allelic diversity and copy number in both MHC classes in the common buzzard

Reconstructing Macroevolutionary Patterns in Avian MHC Architecture With Genomic Data

Ancient duplication, coevolution, and selection at the MHC class IIA and IIB genes of birds

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