Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow

Abstract Parasites can exert strong selective pressures on their hosts and influence the evolution of host immunity. While several studies have examined the genetic basis for parasite resistance, the role of epigenetics in the immune response to parasites is less understood. Yet, epigenetic modifica...

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Main Authors: Sarah L. Lundregan, Hannu Mäkinen, Amberly Buer, Håkon Holand, Henrik Jensen, Arild Husby
Format: Article
Language:English
Published: Wiley 2022-11-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.9539
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author Sarah L. Lundregan
Hannu Mäkinen
Amberly Buer
Håkon Holand
Henrik Jensen
Arild Husby
author_facet Sarah L. Lundregan
Hannu Mäkinen
Amberly Buer
Håkon Holand
Henrik Jensen
Arild Husby
author_sort Sarah L. Lundregan
collection DOAJ
description Abstract Parasites can exert strong selective pressures on their hosts and influence the evolution of host immunity. While several studies have examined the genetic basis for parasite resistance, the role of epigenetics in the immune response to parasites is less understood. Yet, epigenetic modifications, such as changes in DNA methylation, may allow species to respond rapidly to parasite prevalence or virulence. To test the role of DNA methylation in relation to parasite infection, we examined genome‐wide DNA methylation before and during infection by a parasitic nematode, Syngamus trachea, in a natural population of house sparrows (Passer domesticus) using reduced representation bisulfite sequencing (RRBS). We found that DNA methylation levels were slightly lower in infected house sparrows, and we identified candidate genes relating to the initial immune response, activation of innate and adaptive immunity, and mucus membrane functional integrity that were differentially methylated between infected and control birds. Subsequently, we used methylation‐sensitive high‐resolution melting (MS‐HRM) analyses to verify the relationship between methylation proportion and S. trachea infection status at two candidate genes in a larger sample dataset. We found that methylation level at NR1D1, but not CLDN22, remained related to infection status and that juvenile recruitment probability was positively related to methylation level at NR1D1. This underscores the importance of performing follow‐up studies on candidate genes. Our findings demonstrate that plasticity in the immune response to parasites can be epigenetically mediated and highlight the potential for epigenetic studies in natural populations to provide further mechanistic insight into host–parasite interactions.
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spelling doaj.art-6d6804e14910442dada952346fd010542022-12-22T03:46:30ZengWileyEcology and Evolution2045-77582022-11-011211n/an/a10.1002/ece3.9539Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrowSarah L. Lundregan0Hannu Mäkinen1Amberly Buer2Håkon Holand3Henrik Jensen4Arild Husby5Department of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayDepartment of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayDepartment of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayDepartment of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayDepartment of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayDepartment of Biology, Centre for Biodiversity Dynamics Norwegian University of Science and Technology Trondheim NorwayAbstract Parasites can exert strong selective pressures on their hosts and influence the evolution of host immunity. While several studies have examined the genetic basis for parasite resistance, the role of epigenetics in the immune response to parasites is less understood. Yet, epigenetic modifications, such as changes in DNA methylation, may allow species to respond rapidly to parasite prevalence or virulence. To test the role of DNA methylation in relation to parasite infection, we examined genome‐wide DNA methylation before and during infection by a parasitic nematode, Syngamus trachea, in a natural population of house sparrows (Passer domesticus) using reduced representation bisulfite sequencing (RRBS). We found that DNA methylation levels were slightly lower in infected house sparrows, and we identified candidate genes relating to the initial immune response, activation of innate and adaptive immunity, and mucus membrane functional integrity that were differentially methylated between infected and control birds. Subsequently, we used methylation‐sensitive high‐resolution melting (MS‐HRM) analyses to verify the relationship between methylation proportion and S. trachea infection status at two candidate genes in a larger sample dataset. We found that methylation level at NR1D1, but not CLDN22, remained related to infection status and that juvenile recruitment probability was positively related to methylation level at NR1D1. This underscores the importance of performing follow‐up studies on candidate genes. Our findings demonstrate that plasticity in the immune response to parasites can be epigenetically mediated and highlight the potential for epigenetic studies in natural populations to provide further mechanistic insight into host–parasite interactions.https://doi.org/10.1002/ece3.9539DNA methylationepigeneticsimmunityparasitepasserineRRBS
spellingShingle Sarah L. Lundregan
Hannu Mäkinen
Amberly Buer
Håkon Holand
Henrik Jensen
Arild Husby
Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
Ecology and Evolution
DNA methylation
epigenetics
immunity
parasite
passerine
RRBS
title Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
title_full Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
title_fullStr Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
title_full_unstemmed Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
title_short Infection by a helminth parasite is associated with changes in DNA methylation in the house sparrow
title_sort infection by a helminth parasite is associated with changes in dna methylation in the house sparrow
topic DNA methylation
epigenetics
immunity
parasite
passerine
RRBS
url https://doi.org/10.1002/ece3.9539
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