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Meta-analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species.

ABSTRACT: Pathogen-mediated selection and sexual selection are important drivers of evolution. Both processes are known to target genes of the major histocompatibility complex (MHC), a gene family encoding cell-surface proteins that display pathogen peptides to the immune system. The MHC is also a model for understanding processes such as gene duplication and trans-species allele sharing. The class II MHC protein is a heterodimer whose peptide-binding groove is encoded by an MHC-IIA gene and an MHC-IIB gene. However, our literature review found that class II MHC papers on infectious disease or sexual selection included IIA data only 18% and 9% of the time, respectively. To assess whether greater emphasis on MHC-IIA is warranted, we analysed MHC-IIA sequence data from 50 species of vertebrates (fish, amphibians, birds, mammals) to test for polymorphism and positive selection. We found that the number of MHC-IIA alleles within a species was often high, and covaried with sample size and number of MHC-IIA genes assayed. While MHC-IIA variability tended to be lower than that of MHC-IIB, the difference was only ~25%, with ~3 fewer IIA alleles than IIB. Furthermore, the unexpectedly high MHC-IIA variability showed clear signatures of positive selection in most species, and positive selection on MHC-IIA was stronger in fish than in other surveyed vertebrate groups. Our findings underscore that MHC-IIA can be an important target of selection. Future studies should therefore expand the characterization of MHC-IIA at both allelic and genomic scales, and incorporate MHC-IIA into models of fitness consequences of MHC variation.

SUBMITTER: Dearborn DC

PROVIDER: S-EPMC9729452 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Meta-analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species.

Dearborn Donald C DC Warren Sophie S Hailer Frank F

Molecular ecology 20221019 24

Pathogen-mediated selection and sexual selection are important drivers of evolution. Both processes are known to target genes of the major histocompatibility complex (MHC), a gene family encoding cell-surface proteins that display pathogen peptides to the immune system. The MHC is also a model for understanding processes such as gene duplication and trans-species allele sharing. The class II MHC protein is a heterodimer whose peptide-binding groove is encoded by an MHC-IIA gene and an MHC-IIB ge ...[more]

PMID: 36208104

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Project description:Genetic diversity is one of the pillars of conservation biology research. High genetic diversity and abundant genetic variation in an organism may be suggestive of capacity to adapt to various environmental changes. The major histocompatibility complex (MHC) is known to be highly polymorphic and plays an important role in immune function. It is also considered an ideal model system to investigate genetic diversity in wildlife populations. The Rufous-backed Bunting (Emberiza jankowskii) is an endangered species that has experienced a sharp decline in both population and habitat size. Many historically significant populations are no longer present in previously populated regions, with only three breeding populations present in Inner Mongolia (i.e., the Aolunhua, Gahaitu and Lubei557 populations). Efforts focused on facilitating the conservation of the Rufous-backed Bunting (Emberiza jankowskii) are becoming increasingly important. However, the genetic diversity of E. jankowskii has not been investigated. In the present study, polymorphism in exon 2 of the MHCIIB of E. jankowskii was investigated. This polymorphism was subsequently compared with a related species, the Meadow Bunting (Emberiza cioides). A total of 1.59 alleles/individual were detected in E. jankowskii and 1.73 alleles/individual were identified in E. cioides. The maximum number of alleles per individual from the three E. jankowskii populations suggest the existence of at least three functional loci, while the maximum number of alleles per individual from the three E. cioides populations suggest the presence of at least four functional loci. Two of the alleles were shared between the E. jankowskii and E. cioides. Among the 12 unique alleles identified in E. jankowskii, 10.17 segregating sites per allele were detected, and the nucleotide diversity was 0.1865. Among the 17 unique alleles identified in E. cioides, eight segregating sites per allele were detected, and the nucleotide diversity was 0.1667. Overall, compared to other passerine birds, a relatively low level of MHC polymorphism was revealed in E. jankowskii, which was similar to that in E. cioides. Positive selection was detected by PAML/SLAC/FEL analyses in the region encoding the peptide-binding region in both species, and no recombination was detected. Phylogenetic analysis showed that the alleles from E. jankowskii and E. cioides belong to the same clade and the two species shared similar alleles, suggesting the occurrence of a trans-species polymorphism between the two Emberiza species.

Dataset Information

Meta-analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species.

Publications

Meta-analysis of major histocompatibility complex (MHC) class IIA reveals polymorphism and positive selection in many vertebrate species.

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