Balancing selection on the complement system of a wild rodent

BACKGROUND: Selection pressure exerted by pathogens can influence patterns of genetic diversity in the host. In the immune system especially, numerous genes encode proteins involved in antagonistic interactions with pathogens, paving the way for coevolution that results in increased genetic diversit...

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Autores principales: Nandakumar, Mridula, Lundberg, Max, Carlsson, Fredric, Råberg, Lars
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10214634/
https://www.ncbi.nlm.nih.gov/pubmed/37231383
http://dx.doi.org/10.1186/s12862-023-02122-0
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author Nandakumar, Mridula
Lundberg, Max
Carlsson, Fredric
Råberg, Lars
author_facet Nandakumar, Mridula
Lundberg, Max
Carlsson, Fredric
Råberg, Lars
author_sort Nandakumar, Mridula
collection PubMed
description BACKGROUND: Selection pressure exerted by pathogens can influence patterns of genetic diversity in the host. In the immune system especially, numerous genes encode proteins involved in antagonistic interactions with pathogens, paving the way for coevolution that results in increased genetic diversity as a consequence of balancing selection. The complement system is a key component of innate immunity. Many complement proteins interact directly with pathogens, either by recognising pathogen molecules for complement activation, or by serving as targets of pathogen immune evasion mechanisms. Complement genes can therefore be expected to be important targets of pathogen-mediated balancing selection, but analyses of such selection on this part of the immune system have been limited. RESULTS: Using a population sample of whole-genome resequencing data from wild bank voles (n = 31), we estimated the extent of genetic diversity and tested for signatures of balancing selection in multiple complement genes (n = 44). Complement genes showed higher values of standardised β (a statistic expected to be high under balancing selection) than the genome-wide average of protein coding genes. One complement gene, FCNA, a pattern recognition molecule that interacts directly with pathogens, was found to have a signature of balancing selection, as indicated by the Hudson-Kreitman-Aguadé test (HKA) test. Scans for localised signatures of balancing selection in this gene indicated that the target of balancing selection was found in exonic regions involved in ligand binding. CONCLUSION: The present study adds to the growing evidence that balancing selection may be an important evolutionary force on components of the innate immune system. The identified target in the complement system typifies the expectation that balancing selection acts on genes encoding proteins involved in direct interactions with pathogens. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02122-0.
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spelling pubmed-102146342023-05-27 Balancing selection on the complement system of a wild rodent Nandakumar, Mridula Lundberg, Max Carlsson, Fredric Råberg, Lars BMC Ecol Evol Research BACKGROUND: Selection pressure exerted by pathogens can influence patterns of genetic diversity in the host. In the immune system especially, numerous genes encode proteins involved in antagonistic interactions with pathogens, paving the way for coevolution that results in increased genetic diversity as a consequence of balancing selection. The complement system is a key component of innate immunity. Many complement proteins interact directly with pathogens, either by recognising pathogen molecules for complement activation, or by serving as targets of pathogen immune evasion mechanisms. Complement genes can therefore be expected to be important targets of pathogen-mediated balancing selection, but analyses of such selection on this part of the immune system have been limited. RESULTS: Using a population sample of whole-genome resequencing data from wild bank voles (n = 31), we estimated the extent of genetic diversity and tested for signatures of balancing selection in multiple complement genes (n = 44). Complement genes showed higher values of standardised β (a statistic expected to be high under balancing selection) than the genome-wide average of protein coding genes. One complement gene, FCNA, a pattern recognition molecule that interacts directly with pathogens, was found to have a signature of balancing selection, as indicated by the Hudson-Kreitman-Aguadé test (HKA) test. Scans for localised signatures of balancing selection in this gene indicated that the target of balancing selection was found in exonic regions involved in ligand binding. CONCLUSION: The present study adds to the growing evidence that balancing selection may be an important evolutionary force on components of the innate immune system. The identified target in the complement system typifies the expectation that balancing selection acts on genes encoding proteins involved in direct interactions with pathogens. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02122-0. BioMed Central 2023-05-25 /pmc/articles/PMC10214634/ /pubmed/37231383 http://dx.doi.org/10.1186/s12862-023-02122-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nandakumar, Mridula
Lundberg, Max
Carlsson, Fredric
Råberg, Lars
Balancing selection on the complement system of a wild rodent
title Balancing selection on the complement system of a wild rodent
title_full Balancing selection on the complement system of a wild rodent
title_fullStr Balancing selection on the complement system of a wild rodent
title_full_unstemmed Balancing selection on the complement system of a wild rodent
title_short Balancing selection on the complement system of a wild rodent
title_sort balancing selection on the complement system of a wild rodent
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10214634/
https://www.ncbi.nlm.nih.gov/pubmed/37231383
http://dx.doi.org/10.1186/s12862-023-02122-0
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