Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose

Schubert, Nadine; Nichols, Hazel; Mwanguhya, Francis; Businge, Robert; Kyambulima, Solomon; Mwesige, Kenneth; Cant, Michael A.; Winternitz, Jamie C.

doi:10.1186/s12862-025-02456-x

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Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose

Nadine Schubert

, Hazel Nichols

, Francis Mwanguhya, Robert Businge, Solomon Kyambulima, Kenneth Mwesige, Michael A. Cant, Jamie C. Winternitz

BMC Ecology and Evolution, Volume: 25, Issue: 1

Swansea University Author: Hazel Nichols

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DOI (Published version): 10.1186/s12862-025-02456-x

Abstract

BackgroundThe major histocompatibility complex’s (MHC) role in the vertebrate adaptive immune response and its exceptional polymorphism make it a key target for studying adaptive gene evolution. However, studies on carnivore MHC often focus on populations with severe bottlenecks or conservation conc...

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Published in:	BMC Ecology and Evolution
ISSN:	2730-7182
Published:	Springer Science and Business Media LLC 2025
Online Access:	Check full text
URI:	https://cronfa.swan.ac.uk/Record/cronfa70660

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Furthermore, many studies focus on one MHC class and do not cover the whole peptide binding groove of the MHC molecule. Here, we characterize MHC class I (MHC-I) exon 2 and 3, encoding the α1- and α2-domains, as well as MHC-II DRB exon 2 for a large sample (N = 285–384) of a wild carnivore of least conservation concern but with high levels of inbreeding, the banded mongoose.ResultsMHC-I showed higher allelic and supertype diversity and polymorphism compared to MHC-II, consistent with findings in humans where MHC-I experiences stronger diversifying selection. MHC-I exon 3 exhibited the lowest diversity, likely due to its specific role in forming the peptide binding groove. Diversifying selection was stronger on MHC-I exon 2 (α1 domain) than exon 3 (α2 domain). Despite frequent inbreeding, banded mongooses showed MHC diversity comparable to other carnivores of least concern using phylogenetic mixed models. Phylogenetic analysis indicated a longer evolutionary trajectory for MHC-II compared to MHC-I and species-specific gene duplication of nonclassical MHC-I sequences clustering with classical sequences. Trans-species polymorphism in nonclassical MHC-I sequences suggested homology or convergent evolution.ConclusionsThis study is the first to characterize both MHC classes of a social, wild carnivore using high-throughput sequencing and a large sample size. Despite frequent inbreeding, banded mongooses exhibit MHC diversity comparable to other carnivores of least conservation concern, challenging assumptions that inbreeding universally reduces genetic diversity. Higher diversity and selection on MHC-I exon 2 emphasize its role in immune defense, while lower diversity in exon 3 highlights functional divergence between the exons. The longer evolutionary trajectory of MHC-II reveals differences in dynamics between MHC classes. Species-specific gene duplication and trans-species polymorphism in nonclassical MHC-I sequences suggest complex evolutionary mechanisms. These findings advance understanding of MHC evolution in wild carnivores, with implications for conservation genetics, particularly regarding the effects of social structure and inbreeding on immune gene diversity.</abstract><type>Journal Article</type><journal>BMC Ecology and Evolution</journal><volume>25</volume><journalNumber>1</journalNumber><paginationStart/><paginationEnd/><publisher>Springer Science and Business Media LLC</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2730-7182</issnElectronic><keywords>MHC; Genetic diversity; Mungos mungo; Balancing selection; Trans-species polymorphism; Carnivore; Phylogenetic mixed model</keywords><publishedDay>14</publishedDay><publishedMonth>10</publishedMonth><publishedYear>2025</publishedYear><publishedDate>2025-10-14</publishedDate><doi>10.1186/s12862-025-02456-x</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences Geography and Physics School</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BGPS</DepartmentCode><institution>Swansea University</institution><apcterm>Another institution paid the OA fee</apcterm><funders>Open Access funding enabled and organized by Projekt DEAL. This work was supported by the German Research Foundation (DFG) – Project number 416495992 to JW. JW was supported by the DFG as part of the SFB TRR 212 (NC³) – Project numbers 316099922 and 396780709. HJN was supported by an Alexander von Humboldt Foundation Research Fellowship and a Leverhulme Trust International Fellowship (grant reference: IAF-2018-006). The funding bodies played no role in the design of the study and collection, analysis, interpretation of data, and in writing the manuscript. 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spelling	2025-12-08T12:11:50.6553423 v2 70660 2025-10-14 Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose 43ba12986bd7754484874c73eed0ebfe 0000-0002-4455-6065 Hazel Nichols Hazel Nichols true false 2025-10-14 BGPS BackgroundThe major histocompatibility complex’s (MHC) role in the vertebrate adaptive immune response and its exceptional polymorphism make it a key target for studying adaptive gene evolution. However, studies on carnivore MHC often focus on populations with severe bottlenecks or conservation concerns, leading to small sample sizes and unreliable generalizations about MHC diversity. Furthermore, many studies focus on one MHC class and do not cover the whole peptide binding groove of the MHC molecule. Here, we characterize MHC class I (MHC-I) exon 2 and 3, encoding the α1- and α2-domains, as well as MHC-II DRB exon 2 for a large sample (N = 285–384) of a wild carnivore of least conservation concern but with high levels of inbreeding, the banded mongoose.ResultsMHC-I showed higher allelic and supertype diversity and polymorphism compared to MHC-II, consistent with findings in humans where MHC-I experiences stronger diversifying selection. MHC-I exon 3 exhibited the lowest diversity, likely due to its specific role in forming the peptide binding groove. Diversifying selection was stronger on MHC-I exon 2 (α1 domain) than exon 3 (α2 domain). Despite frequent inbreeding, banded mongooses showed MHC diversity comparable to other carnivores of least concern using phylogenetic mixed models. Phylogenetic analysis indicated a longer evolutionary trajectory for MHC-II compared to MHC-I and species-specific gene duplication of nonclassical MHC-I sequences clustering with classical sequences. Trans-species polymorphism in nonclassical MHC-I sequences suggested homology or convergent evolution.ConclusionsThis study is the first to characterize both MHC classes of a social, wild carnivore using high-throughput sequencing and a large sample size. Despite frequent inbreeding, banded mongooses exhibit MHC diversity comparable to other carnivores of least conservation concern, challenging assumptions that inbreeding universally reduces genetic diversity. Higher diversity and selection on MHC-I exon 2 emphasize its role in immune defense, while lower diversity in exon 3 highlights functional divergence between the exons. The longer evolutionary trajectory of MHC-II reveals differences in dynamics between MHC classes. Species-specific gene duplication and trans-species polymorphism in nonclassical MHC-I sequences suggest complex evolutionary mechanisms. These findings advance understanding of MHC evolution in wild carnivores, with implications for conservation genetics, particularly regarding the effects of social structure and inbreeding on immune gene diversity. Journal Article BMC Ecology and Evolution 25 1 Springer Science and Business Media LLC 2730-7182 MHC; Genetic diversity; Mungos mungo; Balancing selection; Trans-species polymorphism; Carnivore; Phylogenetic mixed model 14 10 2025 2025-10-14 10.1186/s12862-025-02456-x COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University Another institution paid the OA fee Open Access funding enabled and organized by Projekt DEAL. This work was supported by the German Research Foundation (DFG) – Project number 416495992 to JW. JW was supported by the DFG as part of the SFB TRR 212 (NC³) – Project numbers 316099922 and 396780709. HJN was supported by an Alexander von Humboldt Foundation Research Fellowship and a Leverhulme Trust International Fellowship (grant reference: IAF-2018-006). The funding bodies played no role in the design of the study and collection, analysis, interpretation of data, and in writing the manuscript. We acknowledge financial support from the Open Access Publication Fund of Universität Hamburg. 2025-12-08T12:11:50.6553423 2025-10-14T12:23:53.8061825 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Nadine Schubert 0000-0001-6131-3543 1 Hazel Nichols 0000-0002-4455-6065 2 Francis Mwanguhya 3 Robert Businge 4 Solomon Kyambulima 5 Kenneth Mwesige 6 Michael A. Cant 7 Jamie C. Winternitz 0000-0002-1113-9126 8 70660__35787__ed36f32b9a6944fd82d67b8a49c284c3.pdf 70660.VoR.pdf 2025-12-08T12:09:16.9131323 Output 5748069 application/pdf Version of Record true © The Author(s) 2025. This article is licensed under a Creative Commons Attribution 4.0 International License. true eng http://creativecommons.org/licenses/by/4.0/
title	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
spellingShingle	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose Hazel Nichols
title_short	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
title_full	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
title_fullStr	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
title_full_unstemmed	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
title_sort	Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose
author_id_str_mv	43ba12986bd7754484874c73eed0ebfe
author_id_fullname_str_mv	43ba12986bd7754484874c73eed0ebfe_***_Hazel Nichols
author	Hazel Nichols
author2	Nadine Schubert Hazel Nichols Francis Mwanguhya Robert Businge Solomon Kyambulima Kenneth Mwesige Michael A. Cant Jamie C. Winternitz
format	Journal article
container_title	BMC Ecology and Evolution
container_volume	25
container_issue	1
publishDate	2025
institution	Swansea University
issn	2730-7182
doi_str_mv	10.1186/s12862-025-02456-x
publisher	Springer Science and Business Media LLC
college_str	Faculty of Science and Engineering
hierarchytype
hierarchy_top_id	facultyofscienceandengineering
hierarchy_top_title	Faculty of Science and Engineering
hierarchy_parent_id	facultyofscienceandengineering
hierarchy_parent_title	Faculty of Science and Engineering
department_str	School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str	1
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description	BackgroundThe major histocompatibility complex’s (MHC) role in the vertebrate adaptive immune response and its exceptional polymorphism make it a key target for studying adaptive gene evolution. However, studies on carnivore MHC often focus on populations with severe bottlenecks or conservation concerns, leading to small sample sizes and unreliable generalizations about MHC diversity. Furthermore, many studies focus on one MHC class and do not cover the whole peptide binding groove of the MHC molecule. Here, we characterize MHC class I (MHC-I) exon 2 and 3, encoding the α1- and α2-domains, as well as MHC-II DRB exon 2 for a large sample (N = 285–384) of a wild carnivore of least conservation concern but with high levels of inbreeding, the banded mongoose.ResultsMHC-I showed higher allelic and supertype diversity and polymorphism compared to MHC-II, consistent with findings in humans where MHC-I experiences stronger diversifying selection. MHC-I exon 3 exhibited the lowest diversity, likely due to its specific role in forming the peptide binding groove. Diversifying selection was stronger on MHC-I exon 2 (α1 domain) than exon 3 (α2 domain). Despite frequent inbreeding, banded mongooses showed MHC diversity comparable to other carnivores of least concern using phylogenetic mixed models. Phylogenetic analysis indicated a longer evolutionary trajectory for MHC-II compared to MHC-I and species-specific gene duplication of nonclassical MHC-I sequences clustering with classical sequences. Trans-species polymorphism in nonclassical MHC-I sequences suggested homology or convergent evolution.ConclusionsThis study is the first to characterize both MHC classes of a social, wild carnivore using high-throughput sequencing and a large sample size. Despite frequent inbreeding, banded mongooses exhibit MHC diversity comparable to other carnivores of least conservation concern, challenging assumptions that inbreeding universally reduces genetic diversity. Higher diversity and selection on MHC-I exon 2 emphasize its role in immune defense, while lower diversity in exon 3 highlights functional divergence between the exons. The longer evolutionary trajectory of MHC-II reveals differences in dynamics between MHC classes. Species-specific gene duplication and trans-species polymorphism in nonclassical MHC-I sequences suggest complex evolutionary mechanisms. These findings advance understanding of MHC evolution in wild carnivores, with implications for conservation genetics, particularly regarding the effects of social structure and inbreeding on immune gene diversity.
published_date	2025-10-14T05:30:08Z
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score	11.089572

Inbreeding does not reduce major histocompatibility complex diversity in the banded mongoose

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