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Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae

BACKGROUND: As pathogens that circumvent the host immune response are favoured by selection, so are host alleles that reduce parasite load. Such evolutionary processes leave their signature on the genes involved. Deciphering modes of selection operating on immune genes might reveal the nature of hos...

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Autores principales: Lehmann, Tovi, Hume, Jen C. C., Licht, Monica, Burns, Christopher S., Wollenberg, Kurt, Simard, Fred, Ribeiro, Jose' M. C.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2642720/
https://www.ncbi.nlm.nih.gov/pubmed/19234606
http://dx.doi.org/10.1371/journal.pone.0004549
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author Lehmann, Tovi
Hume, Jen C. C.
Licht, Monica
Burns, Christopher S.
Wollenberg, Kurt
Simard, Fred
Ribeiro, Jose' M. C.
author_facet Lehmann, Tovi
Hume, Jen C. C.
Licht, Monica
Burns, Christopher S.
Wollenberg, Kurt
Simard, Fred
Ribeiro, Jose' M. C.
author_sort Lehmann, Tovi
collection PubMed
description BACKGROUND: As pathogens that circumvent the host immune response are favoured by selection, so are host alleles that reduce parasite load. Such evolutionary processes leave their signature on the genes involved. Deciphering modes of selection operating on immune genes might reveal the nature of host-pathogen interactions and factors that govern susceptibility in host populations. Such understanding would have important public health implications. METHODOLOGY/FINDINGS: We analyzed polymorphisms in four mosquito immune genes (SP14D1, GNBP, defensin, and gambicin) to decipher selection effects, presumably mediated by pathogens. Using samples of Anopheles arabiensis, An. quadriannulatus and four An. gambiae populations, as well as published sequences from other Culicidae, we contrasted patterns of polymorphisms between different functional units of the same gene within and between populations. Our results revealed selection signatures operating on different time scales. At the most recent time scale, within-population diversity revealed purifying selection. Between populations and between species variation revealed reduced differentiation (GNBP and gambicin) at coding vs. noncoding- regions, consistent with balancing selection. McDonald-Kreitman tests between An. quadriannulatus and both sibling species revealed higher fixation rate of synonymous than nonsynonymous substitutions (GNBP) in accordance with frequency dependent balancing selection. At the longest time scale (>100 my), PAML analysis using distant Culicid taxa revealed positive selection at one codon in gambicin. Patterns of genetic variation were independent of exposure to human pathogens. SIGNIFICANCE AND CONCLUSIONS: Purifying selection is the most common form of selection operating on immune genes as it was detected on a contemporary time scale on all genes. Selection for “hypervariability” was not detected, but negative balancing selection, detected at a recent evolutionary time scale between sibling species may be rather common. Detection of positive selection at the deepest evolutionary time scale suggests that it occurs infrequently, possibly in association with speciation events. Our results provided no evidence to support the hypothesis that selection was mediated by pathogens that are transmitted to humans.
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spelling pubmed-26427202009-02-23 Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae Lehmann, Tovi Hume, Jen C. C. Licht, Monica Burns, Christopher S. Wollenberg, Kurt Simard, Fred Ribeiro, Jose' M. C. PLoS One Research Article BACKGROUND: As pathogens that circumvent the host immune response are favoured by selection, so are host alleles that reduce parasite load. Such evolutionary processes leave their signature on the genes involved. Deciphering modes of selection operating on immune genes might reveal the nature of host-pathogen interactions and factors that govern susceptibility in host populations. Such understanding would have important public health implications. METHODOLOGY/FINDINGS: We analyzed polymorphisms in four mosquito immune genes (SP14D1, GNBP, defensin, and gambicin) to decipher selection effects, presumably mediated by pathogens. Using samples of Anopheles arabiensis, An. quadriannulatus and four An. gambiae populations, as well as published sequences from other Culicidae, we contrasted patterns of polymorphisms between different functional units of the same gene within and between populations. Our results revealed selection signatures operating on different time scales. At the most recent time scale, within-population diversity revealed purifying selection. Between populations and between species variation revealed reduced differentiation (GNBP and gambicin) at coding vs. noncoding- regions, consistent with balancing selection. McDonald-Kreitman tests between An. quadriannulatus and both sibling species revealed higher fixation rate of synonymous than nonsynonymous substitutions (GNBP) in accordance with frequency dependent balancing selection. At the longest time scale (>100 my), PAML analysis using distant Culicid taxa revealed positive selection at one codon in gambicin. Patterns of genetic variation were independent of exposure to human pathogens. SIGNIFICANCE AND CONCLUSIONS: Purifying selection is the most common form of selection operating on immune genes as it was detected on a contemporary time scale on all genes. Selection for “hypervariability” was not detected, but negative balancing selection, detected at a recent evolutionary time scale between sibling species may be rather common. Detection of positive selection at the deepest evolutionary time scale suggests that it occurs infrequently, possibly in association with speciation events. Our results provided no evidence to support the hypothesis that selection was mediated by pathogens that are transmitted to humans. Public Library of Science 2009-02-23 /pmc/articles/PMC2642720/ /pubmed/19234606 http://dx.doi.org/10.1371/journal.pone.0004549 Text en This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Lehmann, Tovi
Hume, Jen C. C.
Licht, Monica
Burns, Christopher S.
Wollenberg, Kurt
Simard, Fred
Ribeiro, Jose' M. C.
Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title_full Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title_fullStr Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title_full_unstemmed Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title_short Molecular Evolution of Immune Genes in the Malaria Mosquito Anopheles gambiae
title_sort molecular evolution of immune genes in the malaria mosquito anopheles gambiae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2642720/
https://www.ncbi.nlm.nih.gov/pubmed/19234606
http://dx.doi.org/10.1371/journal.pone.0004549
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