Ancient diversity in host-parasite interaction genes in a model parasitic nematode

Abstract Host-parasite interactions exert strong selection pressures on the genomes of both host and parasite. These interactions can lead to negative frequency-dependent selection, a form of balancing selection that is hypothesised to explain the high levels of polymorphism seen in many host immune...

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Main Authors: Lewis Stevens, Isaac Martínez-Ugalde, Erna King, Martin Wagah, Dominic Absolon, Rowan Bancroft, Pablo Gonzalez de la Rosa, Jessica L. Hall, Manuela Kieninger, Agnieszka Kloch, Sarah Pelan, Elaine Robertson, Amy B. Pedersen, Cei Abreu-Goodger, Amy H. Buck, Mark Blaxter
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-43556-w
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author Lewis Stevens
Isaac Martínez-Ugalde
Erna King
Martin Wagah
Dominic Absolon
Rowan Bancroft
Pablo Gonzalez de la Rosa
Jessica L. Hall
Manuela Kieninger
Agnieszka Kloch
Sarah Pelan
Elaine Robertson
Amy B. Pedersen
Cei Abreu-Goodger
Amy H. Buck
Mark Blaxter
author_facet Lewis Stevens
Isaac Martínez-Ugalde
Erna King
Martin Wagah
Dominic Absolon
Rowan Bancroft
Pablo Gonzalez de la Rosa
Jessica L. Hall
Manuela Kieninger
Agnieszka Kloch
Sarah Pelan
Elaine Robertson
Amy B. Pedersen
Cei Abreu-Goodger
Amy H. Buck
Mark Blaxter
author_sort Lewis Stevens
collection DOAJ
description Abstract Host-parasite interactions exert strong selection pressures on the genomes of both host and parasite. These interactions can lead to negative frequency-dependent selection, a form of balancing selection that is hypothesised to explain the high levels of polymorphism seen in many host immune and parasite antigen loci. Here, we sequence the genomes of several individuals of Heligmosomoides bakeri, a model parasite of house mice, and Heligmosomoides polygyrus, a closely related parasite of wood mice. Although H. bakeri is commonly referred to as H. polygyrus in the literature, their genomes show levels of divergence that are consistent with at least a million years of independent evolution. The genomes of both species contain hyper-divergent haplotypes that are enriched for proteins that interact with the host immune response. Many of these haplotypes originated prior to the divergence between H. bakeri and H. polygyrus, suggesting that they have been maintained by long-term balancing selection. Together, our results suggest that the selection pressures exerted by the host immune response have played a key role in shaping patterns of genetic diversity in the genomes of parasitic nematodes.
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spelling doaj.art-11ee01788db84224a4f03e8a611535fa2023-12-03T12:28:11ZengNature PortfolioNature Communications2041-17232023-11-0114111910.1038/s41467-023-43556-wAncient diversity in host-parasite interaction genes in a model parasitic nematodeLewis Stevens0Isaac Martínez-Ugalde1Erna King2Martin Wagah3Dominic Absolon4Rowan Bancroft5Pablo Gonzalez de la Rosa6Jessica L. Hall7Manuela Kieninger8Agnieszka Kloch9Sarah Pelan10Elaine Robertson11Amy B. Pedersen12Cei Abreu-Goodger13Amy H. Buck14Mark Blaxter15Tree of Life, Wellcome Sanger InstituteInstitute of Ecology and Evolution, School of Biological Sciences, University of EdinburghTree of Life, Wellcome Sanger InstituteTree of Life, Wellcome Sanger InstituteTree of Life, Wellcome Sanger InstituteInstitute of Ecology and Evolution, School of Biological Sciences, University of EdinburghTree of Life, Wellcome Sanger InstituteInstitute of Ecology and Evolution, School of Biological Sciences, University of EdinburghTree of Life, Wellcome Sanger InstituteFaculty of Biology, University of WarsawTree of Life, Wellcome Sanger InstituteInstitute of Immunology & Infection Research, School of Biological Sciences, University of EdinburghInstitute of Ecology and Evolution, School of Biological Sciences, University of EdinburghInstitute of Ecology and Evolution, School of Biological Sciences, University of EdinburghInstitute of Immunology & Infection Research, School of Biological Sciences, University of EdinburghTree of Life, Wellcome Sanger InstituteAbstract Host-parasite interactions exert strong selection pressures on the genomes of both host and parasite. These interactions can lead to negative frequency-dependent selection, a form of balancing selection that is hypothesised to explain the high levels of polymorphism seen in many host immune and parasite antigen loci. Here, we sequence the genomes of several individuals of Heligmosomoides bakeri, a model parasite of house mice, and Heligmosomoides polygyrus, a closely related parasite of wood mice. Although H. bakeri is commonly referred to as H. polygyrus in the literature, their genomes show levels of divergence that are consistent with at least a million years of independent evolution. The genomes of both species contain hyper-divergent haplotypes that are enriched for proteins that interact with the host immune response. Many of these haplotypes originated prior to the divergence between H. bakeri and H. polygyrus, suggesting that they have been maintained by long-term balancing selection. Together, our results suggest that the selection pressures exerted by the host immune response have played a key role in shaping patterns of genetic diversity in the genomes of parasitic nematodes.https://doi.org/10.1038/s41467-023-43556-w
spellingShingle Lewis Stevens
Isaac Martínez-Ugalde
Erna King
Martin Wagah
Dominic Absolon
Rowan Bancroft
Pablo Gonzalez de la Rosa
Jessica L. Hall
Manuela Kieninger
Agnieszka Kloch
Sarah Pelan
Elaine Robertson
Amy B. Pedersen
Cei Abreu-Goodger
Amy H. Buck
Mark Blaxter
Ancient diversity in host-parasite interaction genes in a model parasitic nematode
Nature Communications
title Ancient diversity in host-parasite interaction genes in a model parasitic nematode
title_full Ancient diversity in host-parasite interaction genes in a model parasitic nematode
title_fullStr Ancient diversity in host-parasite interaction genes in a model parasitic nematode
title_full_unstemmed Ancient diversity in host-parasite interaction genes in a model parasitic nematode
title_short Ancient diversity in host-parasite interaction genes in a model parasitic nematode
title_sort ancient diversity in host parasite interaction genes in a model parasitic nematode
url https://doi.org/10.1038/s41467-023-43556-w
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