Cargando…
Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics
Major histocompatibility complex (MHC) genes encode proteins crucial for adaptive immunity of vertebrates. Negative frequency‐dependent selection (NFDS), resulting from adaptation of parasites to common MHC types, has been hypothesized to maintain high, functionally relevant polymorphism of MHC, but...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9325469/ https://www.ncbi.nlm.nih.gov/pubmed/35510766 http://dx.doi.org/10.1111/mec.16486 |
_version_ | 1784757059522134016 |
---|---|
author | Migalska, Magdalena Przesmycka, Karolina Alsarraf, Mohammed Bajer, Anna Behnke‐Borowczyk, Jolanta Grzybek, Maciej Behnke, Jerzy M. Radwan, Jacek |
author_facet | Migalska, Magdalena Przesmycka, Karolina Alsarraf, Mohammed Bajer, Anna Behnke‐Borowczyk, Jolanta Grzybek, Maciej Behnke, Jerzy M. Radwan, Jacek |
author_sort | Migalska, Magdalena |
collection | PubMed |
description | Major histocompatibility complex (MHC) genes encode proteins crucial for adaptive immunity of vertebrates. Negative frequency‐dependent selection (NFDS), resulting from adaptation of parasites to common MHC types, has been hypothesized to maintain high, functionally relevant polymorphism of MHC, but demonstration of this relationship has remained elusive. In particular, differentiation of NFDS from fluctuating selection, resulting from changes in parasite communities in time and space (FS), has proved difficult in short‐term studies. Here, we used temporal data, accumulated through long‐term monitoring of helminths infecting bank voles (Myodes glareolus), to test specific predictions of NFDS on MHC class II. Data were collected in three, moderately genetically differentiated subpopulations in Poland, which were characterized by some stable spatiotemporal helminth communities but also events indicating introduction of new species and loss of others. We found a complex association between individual MHC diversity and species richness, where intermediate numbers of DRB supertypes correlated with lowest species richness, but the opposite was true for DQB supertypes—arguing against universal selection for immunogenetic optimality. We also showed that particular MHC supertypes explain a portion of the variance in prevalence and abundance of helminths, but this effect was subpopulation‐specific, which is consistent with both NFDS and FS. Finally, in line with NFDS, we found that certain helminths that have recently colonized or spread in a given subpopulation, more frequently or intensely infected voles with MHC supertypes that have been common in the recent past. Overall, our results highlight complex spatial and temporal patterns of MHC‐parasite associations, the latter being consistent with Red Queen coevolutionary dynamics. |
format | Online Article Text |
id | pubmed-9325469 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93254692022-07-30 Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics Migalska, Magdalena Przesmycka, Karolina Alsarraf, Mohammed Bajer, Anna Behnke‐Borowczyk, Jolanta Grzybek, Maciej Behnke, Jerzy M. Radwan, Jacek Mol Ecol ORIGINAL ARTICLES Major histocompatibility complex (MHC) genes encode proteins crucial for adaptive immunity of vertebrates. Negative frequency‐dependent selection (NFDS), resulting from adaptation of parasites to common MHC types, has been hypothesized to maintain high, functionally relevant polymorphism of MHC, but demonstration of this relationship has remained elusive. In particular, differentiation of NFDS from fluctuating selection, resulting from changes in parasite communities in time and space (FS), has proved difficult in short‐term studies. Here, we used temporal data, accumulated through long‐term monitoring of helminths infecting bank voles (Myodes glareolus), to test specific predictions of NFDS on MHC class II. Data were collected in three, moderately genetically differentiated subpopulations in Poland, which were characterized by some stable spatiotemporal helminth communities but also events indicating introduction of new species and loss of others. We found a complex association between individual MHC diversity and species richness, where intermediate numbers of DRB supertypes correlated with lowest species richness, but the opposite was true for DQB supertypes—arguing against universal selection for immunogenetic optimality. We also showed that particular MHC supertypes explain a portion of the variance in prevalence and abundance of helminths, but this effect was subpopulation‐specific, which is consistent with both NFDS and FS. Finally, in line with NFDS, we found that certain helminths that have recently colonized or spread in a given subpopulation, more frequently or intensely infected voles with MHC supertypes that have been common in the recent past. Overall, our results highlight complex spatial and temporal patterns of MHC‐parasite associations, the latter being consistent with Red Queen coevolutionary dynamics. John Wiley and Sons Inc. 2022-05-18 2022-06 /pmc/articles/PMC9325469/ /pubmed/35510766 http://dx.doi.org/10.1111/mec.16486 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made. |
spellingShingle | ORIGINAL ARTICLES Migalska, Magdalena Przesmycka, Karolina Alsarraf, Mohammed Bajer, Anna Behnke‐Borowczyk, Jolanta Grzybek, Maciej Behnke, Jerzy M. Radwan, Jacek Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title | Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title_full | Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title_fullStr | Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title_full_unstemmed | Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title_short | Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics |
title_sort | long term patterns of association between mhc and helminth burdens in the bank vole support red queen dynamics |
topic | ORIGINAL ARTICLES |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9325469/ https://www.ncbi.nlm.nih.gov/pubmed/35510766 http://dx.doi.org/10.1111/mec.16486 |
work_keys_str_mv | AT migalskamagdalena longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT przesmyckakarolina longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT alsarrafmohammed longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT bajeranna longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT behnkeborowczykjolanta longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT grzybekmaciej longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT behnkejerzym longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics AT radwanjacek longtermpatternsofassociationbetweenmhcandhelminthburdensinthebankvolesupportredqueendynamics |