Population genetic analysis of autophagy and phagocytosis genes in Drosophila melanogaster and D. simulans
Autophagy and phagocytosis are cellular immune mechanisms for internalization and elimination of intracellular and extracellular pathogens. Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We perfo...
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description | Autophagy and phagocytosis are cellular immune mechanisms for internalization and elimination of intracellular and extracellular pathogens. Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We performed population genetic analyses on phagocytosis and autophagy genes in Drosophila melanogaster and D. simulans to test for molecular evolutionary signatures of immune adaptation. We found that phagocytosis and autophagy genes as a whole exhibited an elevated level of haplotype homozygosity in both species. In addition, we detected signatures of recent selection, notably in the Atg14 and Ykt6 genes in D. melanogaster and a pattern of elevated sequence divergence in the genderblind (gb) gene on the D. simulans lineage. These results suggest that the evolution of the host cellular immune system as a whole may be shaped by a dynamic conflict between Drosophila and its pathogens even without pervasive evidence of strong adaptive evolution at the individual gene level. |
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Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We performed population genetic analyses on phagocytosis and autophagy genes in Drosophila melanogaster and D. simulans to test for molecular evolutionary signatures of immune adaptation. We found that phagocytosis and autophagy genes as a whole exhibited an elevated level of haplotype homozygosity in both species. In addition, we detected signatures of recent selection, notably in the Atg14 and Ykt6 genes in D. melanogaster and a pattern of elevated sequence divergence in the genderblind (gb) gene on the D. simulans lineage. These results suggest that the evolution of the host cellular immune system as a whole may be shaped by a dynamic conflict between Drosophila and its pathogens even without pervasive evidence of strong adaptive evolution at the individual gene level.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0205024</identifier><identifier>PMID: 30281656</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Animals ; Autophagy ; Autophagy (Cytology) ; Autophagy - genetics ; Bacteria ; Biological evolution ; Biology and Life Sciences ; Cell death ; Divergence ; Drosophila ; Drosophila melanogaster ; Drosophila melanogaster - cytology ; Drosophila melanogaster - genetics ; Drosophila melanogaster - immunology ; Drosophila Proteins - genetics ; Drosophila simulans - cytology ; Drosophila simulans - genetics ; Drosophila simulans - immunology ; Evolution ; Evolution & development ; Evolution, Molecular ; Genes ; Genetic analysis ; Genetic aspects ; Genetics, Population ; Genomes ; Genomics ; Haplotypes ; Homozygosity ; Immune system ; Insects ; Internalization ; Pathogens ; Phagocytosis ; Phagocytosis - genetics ; Physical Sciences ; Population genetics ; Proteins ; Research and Analysis Methods ; Signatures</subject><ispartof>PloS one, 2018-10, Vol.13 (10), p.e0205024-e0205024</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Im, Lazzaro. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2018 Im, Lazzaro 2018 Im, Lazzaro</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-a173281064b582a2bc0a3bf022674cbb6a65928ea81e20a6faf5aaa316db677d3</citedby><cites>FETCH-LOGICAL-c692t-a173281064b582a2bc0a3bf022674cbb6a65928ea81e20a6faf5aaa316db677d3</cites><orcidid>0000-0001-5733-6072</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6169979/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6169979/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30281656$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Palsson, Arnar</contributor><creatorcontrib>Im, Joo Hyun</creatorcontrib><creatorcontrib>Lazzaro, Brian P</creatorcontrib><title>Population genetic analysis of autophagy and phagocytosis genes in Drosophila melanogaster and D. simulans</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Autophagy and phagocytosis are cellular immune mechanisms for internalization and elimination of intracellular and extracellular pathogens. Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We performed population genetic analyses on phagocytosis and autophagy genes in Drosophila melanogaster and D. simulans to test for molecular evolutionary signatures of immune adaptation. We found that phagocytosis and autophagy genes as a whole exhibited an elevated level of haplotype homozygosity in both species. In addition, we detected signatures of recent selection, notably in the Atg14 and Ykt6 genes in D. melanogaster and a pattern of elevated sequence divergence in the genderblind (gb) gene on the D. simulans lineage. These results suggest that the evolution of the host cellular immune system as a whole may be shaped by a dynamic conflict between Drosophila and its pathogens even without pervasive evidence of strong adaptive evolution at the individual gene level.</description><subject>Adaptation</subject><subject>Animals</subject><subject>Autophagy</subject><subject>Autophagy (Cytology)</subject><subject>Autophagy - genetics</subject><subject>Bacteria</subject><subject>Biological evolution</subject><subject>Biology and Life Sciences</subject><subject>Cell death</subject><subject>Divergence</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - cytology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - immunology</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila simulans - cytology</subject><subject>Drosophila simulans - genetics</subject><subject>Drosophila simulans - 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genetics</topic><topic>Bacteria</topic><topic>Biological evolution</topic><topic>Biology and Life Sciences</topic><topic>Cell death</topic><topic>Divergence</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - cytology</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - immunology</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila simulans - cytology</topic><topic>Drosophila simulans - genetics</topic><topic>Drosophila simulans - immunology</topic><topic>Evolution</topic><topic>Evolution & development</topic><topic>Evolution, Molecular</topic><topic>Genes</topic><topic>Genetic analysis</topic><topic>Genetic aspects</topic><topic>Genetics, Population</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Haplotypes</topic><topic>Homozygosity</topic><topic>Immune system</topic><topic>Insects</topic><topic>Internalization</topic><topic>Pathogens</topic><topic>Phagocytosis</topic><topic>Phagocytosis - genetics</topic><topic>Physical Sciences</topic><topic>Population genetics</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Signatures</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Im, Joo Hyun</creatorcontrib><creatorcontrib>Lazzaro, Brian P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Im, Joo Hyun</au><au>Lazzaro, Brian P</au><au>Palsson, Arnar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Population genetic analysis of autophagy and phagocytosis genes in Drosophila melanogaster and D. simulans</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-10-03</date><risdate>2018</risdate><volume>13</volume><issue>10</issue><spage>e0205024</spage><epage>e0205024</epage><pages>e0205024-e0205024</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Autophagy and phagocytosis are cellular immune mechanisms for internalization and elimination of intracellular and extracellular pathogens. Some pathogens have evolved the ability to inhibit or manipulate these processes, raising the prospect of adaptive reciprocal co-evolution by the host. We performed population genetic analyses on phagocytosis and autophagy genes in Drosophila melanogaster and D. simulans to test for molecular evolutionary signatures of immune adaptation. We found that phagocytosis and autophagy genes as a whole exhibited an elevated level of haplotype homozygosity in both species. In addition, we detected signatures of recent selection, notably in the Atg14 and Ykt6 genes in D. melanogaster and a pattern of elevated sequence divergence in the genderblind (gb) gene on the D. simulans lineage. These results suggest that the evolution of the host cellular immune system as a whole may be shaped by a dynamic conflict between Drosophila and its pathogens even without pervasive evidence of strong adaptive evolution at the individual gene level.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30281656</pmid><doi>10.1371/journal.pone.0205024</doi><tpages>e0205024</tpages><orcidid>https://orcid.org/0000-0001-5733-6072</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation Animals Autophagy Autophagy (Cytology) Autophagy - genetics Bacteria Biological evolution Biology and Life Sciences Cell death Divergence Drosophila Drosophila melanogaster Drosophila melanogaster - cytology Drosophila melanogaster - genetics Drosophila melanogaster - immunology Drosophila Proteins - genetics Drosophila simulans - cytology Drosophila simulans - genetics Drosophila simulans - immunology Evolution Evolution & development Evolution, Molecular Genes Genetic analysis Genetic aspects Genetics, Population Genomes Genomics Haplotypes Homozygosity Immune system Insects Internalization Pathogens Phagocytosis Phagocytosis - genetics Physical Sciences Population genetics Proteins Research and Analysis Methods Signatures |
title | Population genetic analysis of autophagy and phagocytosis genes in Drosophila melanogaster and D. simulans |
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