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Distinct evolutionary trajectories of MHC class I and class II genes in Old World finches and buntings

Abstract

Major histocompatibility complex (MHC) genes code for key proteins of the adaptive immune system, which present antigens from intra-cellular (MHC class I) and extra-cellular (MHC class II) pathogens. Because of their unprecedented diversity, MHC genes have long been an object of scientific interest, but due to methodological difficulties in genotyping of duplicated loci, our knowledge on the evolution of the MHC across different vertebrate lineages is still limited. Here, we compared the evolution of MHC class I and class II genes in three sister clades of common passerine birds, finches (Fringillinae and Carduelinae) and buntings (Emberizidae) using a uniform methodological (genotyping and data processing) approach and uniform sample sizes. Our analyses revealed contrasting evolutionary trajectories of the two MHC classes. We found a stronger signature of pervasive positive selection and higher allele diversity (allele numbers) at the MHC class I than class II. In contrast, MHC class II genes showed greater allele divergence (in terms of nucleotide diversity) and a much stronger recombination (gene conversion) signal. Gene copy numbers at both MHC class I and class II evolved via fluctuating selection and drift (Brownian Motion evolution), but the evolutionary rate was higher at class I. Our study constitutes one of few existing examples, where evolution of MHC class I and class II genes was directly compared using a multi-species approach. We recommend that re-focusing MHC research from single-species and single-class approaches towards multi-species analyses of both MHC classes can substantially increase our understanding MHC evolution in a broad phylogenetic context.

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Fig. 1: MHC gene copy numbers.
Fig. 2: Recombination at the MHC.
Fig. 3: Selection signature at the MHC.
Fig. 4: Phylogenetic clustering of MHC alleles.

Data availability

All sequences generated and used in this study have been deposited in GenBank (Nos: MW740435–MW741429).

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Acknowledgements

We thank all participants of bird ringing projects (Carpatica, Jeziorsko and Operation Baltic) that contributed to sample collection. At two coastal Operation Baltic ringing stations, Mierzeja Wiślana at Vistula Spit, and Bukowo-Kopań, MR, Krzysztof Stępniewski and Michał Redlisiak collected samples and collated bird data. Fieldwork at Operation Baltic was supported by Special Research Facility grants (SPUB) of the Polish Ministry of Science and Higher Education (203733/E-335/SPUB/2016/4) to the Bird Migration Research Station, University of Gdańsk. IC was supported by the Institute of Biology Bucharest, Romanian Academy (RO1567-IBB04/2020). The study was financially supported by the research grant of the National Science Centre in Poland (2015/19/D/NZ8/01310). We thank three anonymous reviewers and the Editor, Barbara Mable, for constructive comments on the earlier draft of the paper.

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Correspondence to Piotr Minias.

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Catching of birds was authorized by the Polish Academy of Sciences, with the approval of the General Directorate for Environmental Protection, Poland. Field research at Bukowo and Mierzeja Wiślana was approved by the Marine Office in Słupsk and Gdańsk, respectively. The study was performed under the permit from the Local Bioethical Committee for Experiments on Animals in Łódź and appropriate Regional Environmental Protection Directorates.

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Minias, P., Włodarczyk, R., Remisiewicz, M. et al. Distinct evolutionary trajectories of MHC class I and class II genes in Old World finches and buntings. Heredity 126, 974–990 (2021). https://doi.org/10.1038/s41437-021-00427-8

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