Widespread Adaptive Introgression of Major Histocompatibility Complex Genes across Vertebrate Hybrid Zones

Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multiallelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate major histocompatibility complex genes are well-established targets of long-term multiallelic balancing selection, so widespread adaptive major histocompatibility complex introgression is expected. Here, we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds, and mammals at advanced stages of speciation. The key prediction of more extensive major histocompatibility complex introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of major histocompatibility complex genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies major histocompatibility complex introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.

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Publication Details

Journal
Molecular Biology and Evolution
Published
2024-09-26
DOI
https://doi.org/10.1093/molbev/msae201
Citations
9
Primary Topic
T-cell and B-cell Immunology
Type
article
Field-Weighted Citation Impact
2.16

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article

Widespread Adaptive Introgression of Major Histocompatibility Complex Genes across Vertebrate Hybrid Zones

Vašek Gvoždík, Lilia Bahri‐Sfar, Darren E. Irwin, Karl P. Phillips et al.
9 citations
Molecular Biology and Evolution
T-cell and B-cell Immunology
2.16
article

Widespread Adaptive Introgression of Major Histocompatibility Complex Genes across Vertebrate Hybrid Zones

Vašek Gvoždík, Lilia Bahri‐Sfar, Darren E. Irwin, Karl P. Phillips, Petr Kotlı́k, Wiesław Babik, Stuart J. E. Baird, Magdalena Migalska, Christophe Dufresnes, Tomasz S. Gaczorek, François Bonhomme, Maciej Pabijan, Yannis Schöneberg, Katarzyna Dudek, Jacek Radwan, Philip McGinnity, Uwe Fritz, Jiřı́ Moravec, Silvia Marková, Libby Natola, A. Souissi
article en
9 citations

Abstract

Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multiallelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate major histocompatibility complex genes are well-established targets of long-term multiallelic balancing selection, so widespread adaptive major histocompatibility complex introgression is expected. Here, we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds, and mammals at advanced stages of speciation. The key prediction of more extensive major histocompatibility complex introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of major histocompatibility complex genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies major histocompatibility complex introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.

Molecular Biology and EvolutionVol. 41(10)
University of New Brunswick (CA), Tunis University (TN), Goethe University Frankfurt (DE), Jagiellonian University (PL), Centre National de la Recherche Scientifique (FR), University of British Columbia (CA), Université de Montpellier (FR), University College Cork (IE), National Museum (CZ), Sorbonne Université (FR), Czech Academy of Sciences, Institute of Animal Physiology and Genetics (CZ), Institut de Systématique, Évolution, Biodiversité (FR), Institut des Sciences de l'Evolution de Montpellier (FR), Senckenberg Biodiversity and Climate Research Centre (DE), Czech Academy of Sciences, Institute of Vertebrate Biology (CZ), Marine Biodiversity Exploitation and Conservation (FR), Université des Antilles (GP), Adam Mickiewicz University in Poznań (PL), Tunis El Manar University (TN)
Grantová Agentura České Republiky, Narodowe Centrum Nauki
Life below water
Openalex Percentile: Top 12%
T-cell and B-cell Immunology
2.16
DOIOpen Access PDFOpenAlex
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