Population Genetics of Anopheles coluzzii Immune Pathways and Genes

Natural selection is expected to drive adaptive evolution in genes involved in host–pathogen interactions. In this study, we use molecular population genetic analyses to understand how natural selection operates on the immune system of Anopheles coluzzii (formerly A. gambiae “M form”). We analyzed p...

Full description

Bibliographic Details
Main Authors:	Rottschaefer, Susan M., Crawford, Jacob E., Riehle, Michelle M., Guelbeogo, Wamdaogo M., Gneme, Awa, Sagnon, N’Fale, Vernick, Kenneth D., Lazzaro, Brian P.
Format:	Online
Language:	English
Published:	Genetics Society of America 2014
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4349087/

id	pubmed-4349087
recordtype	oai_dc
spelling	pubmed-43490872015-03-11 Population Genetics of Anopheles coluzzii Immune Pathways and Genes Rottschaefer, Susan M. Crawford, Jacob E. Riehle, Michelle M. Guelbeogo, Wamdaogo M. Gneme, Awa Sagnon, N’Fale Vernick, Kenneth D. Lazzaro, Brian P. Genetics of Immunity Natural selection is expected to drive adaptive evolution in genes involved in host–pathogen interactions. In this study, we use molecular population genetic analyses to understand how natural selection operates on the immune system of Anopheles coluzzii (formerly A. gambiae “M form”). We analyzed patterns of intraspecific and interspecific genetic variation in 20 immune-related genes and 17 nonimmune genes from a wild population of A. coluzzii and asked if patterns of genetic variation in the immune genes are consistent with pathogen-driven selection shaping the evolution of defense. We found evidence of a balanced polymorphism in CTLMA2, which encodes a C-type lectin involved in regulation of the melanization response. The two CTLMA2 haplotypes, which are distinguished by fixed amino acid differences near the predicted peptide cleavage site, are also segregating in the sister species A. gambiae (“S form”) and A. arabiensis. Comparison of the two haplotypes between species indicates that they were not shared among the species through introgression, but rather that they arose before the species divergence and have been adaptively maintained as a balanced polymorphism in all three species. We additionally found that STAT-B, a retroduplicate of STAT-A, shows strong evidence of adaptive evolution that is consistent with neofunctionalization after duplication. In contrast to the striking patterns of adaptive evolution observed in these Anopheles-specific immune genes, we found no evidence of adaptive evolution in the Toll and Imd innate immune pathways that are orthologously conserved throughout insects. Genes encoding the Imd pathway exhibit high rates of amino acid divergence between Anopheles species but also display elevated amino acid diversity that is consistent with relaxed purifying selection. These results indicate that adaptive coevolution between A. coluzzii and its pathogens is more likely to involve novel or lineage-specific molecular mechanisms than the canonical humoral immune pathways. Genetics Society of America 2014-12-30 /pmc/articles/PMC4349087/ /pubmed/25552603 http://dx.doi.org/10.1534/g3.114.014845 Text en Copyright © 2015 Rottschaefer et al. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Rottschaefer, Susan M. Crawford, Jacob E. Riehle, Michelle M. Guelbeogo, Wamdaogo M. Gneme, Awa Sagnon, N’Fale Vernick, Kenneth D. Lazzaro, Brian P.
spellingShingle	Rottschaefer, Susan M. Crawford, Jacob E. Riehle, Michelle M. Guelbeogo, Wamdaogo M. Gneme, Awa Sagnon, N’Fale Vernick, Kenneth D. Lazzaro, Brian P. Population Genetics of Anopheles coluzzii Immune Pathways and Genes
author_facet	Rottschaefer, Susan M. Crawford, Jacob E. Riehle, Michelle M. Guelbeogo, Wamdaogo M. Gneme, Awa Sagnon, N’Fale Vernick, Kenneth D. Lazzaro, Brian P.
author_sort	Rottschaefer, Susan M.
title	Population Genetics of Anopheles coluzzii Immune Pathways and Genes
title_short	Population Genetics of Anopheles coluzzii Immune Pathways and Genes
title_full	Population Genetics of Anopheles coluzzii Immune Pathways and Genes
title_fullStr	Population Genetics of Anopheles coluzzii Immune Pathways and Genes
title_full_unstemmed	Population Genetics of Anopheles coluzzii Immune Pathways and Genes
title_sort	population genetics of anopheles coluzzii immune pathways and genes
description	Natural selection is expected to drive adaptive evolution in genes involved in host–pathogen interactions. In this study, we use molecular population genetic analyses to understand how natural selection operates on the immune system of Anopheles coluzzii (formerly A. gambiae “M form”). We analyzed patterns of intraspecific and interspecific genetic variation in 20 immune-related genes and 17 nonimmune genes from a wild population of A. coluzzii and asked if patterns of genetic variation in the immune genes are consistent with pathogen-driven selection shaping the evolution of defense. We found evidence of a balanced polymorphism in CTLMA2, which encodes a C-type lectin involved in regulation of the melanization response. The two CTLMA2 haplotypes, which are distinguished by fixed amino acid differences near the predicted peptide cleavage site, are also segregating in the sister species A. gambiae (“S form”) and A. arabiensis. Comparison of the two haplotypes between species indicates that they were not shared among the species through introgression, but rather that they arose before the species divergence and have been adaptively maintained as a balanced polymorphism in all three species. We additionally found that STAT-B, a retroduplicate of STAT-A, shows strong evidence of adaptive evolution that is consistent with neofunctionalization after duplication. In contrast to the striking patterns of adaptive evolution observed in these Anopheles-specific immune genes, we found no evidence of adaptive evolution in the Toll and Imd innate immune pathways that are orthologously conserved throughout insects. Genes encoding the Imd pathway exhibit high rates of amino acid divergence between Anopheles species but also display elevated amino acid diversity that is consistent with relaxed purifying selection. These results indicate that adaptive coevolution between A. coluzzii and its pathogens is more likely to involve novel or lineage-specific molecular mechanisms than the canonical humoral immune pathways.
publisher	Genetics Society of America
publishDate	2014
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4349087/
_version_	1613194997865119744

Population Genetics of Anopheles coluzzii Immune Pathways and Genes

Similar Items