Malaria life cycle intensifies both natural selection and random genetic drift
Analysis of genome sequences of 159 isolates of Plasmodium falciparum from Senegal yields an extraordinarily high proportion (26.85%) of protein-coding genes with the ratio of nonsynonymous to synonymous polymorphism greater than one. This proportion is much greater than observed in other organisms....
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2013-12, Vol.110 (50), p.20129-20134 |
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| creator | Chang, Hsiao-Han Moss, Eli L. Park, Daniel J. Ndiaye, Daouda Mboup, Souleymane Volkman, Sarah K. Sabeti, Pardis C. Wirth, Dyann F. Neafsey, Daniel E. Hartl, Daniel L. |
| description | Analysis of genome sequences of 159 isolates of Plasmodium falciparum from Senegal yields an extraordinarily high proportion (26.85%) of protein-coding genes with the ratio of nonsynonymous to synonymous polymorphism greater than one. This proportion is much greater than observed in other organisms. Also unusual is that the site-frequency spectra of synonymous and non-synonymous polymorphisms are virtually indistinguishable. We hypothesized that the complicated life cycle of malaria parasites might lead to qualitatively different population genetics from that predicted from the classical Wright-Fisher (WF) model, which assumes a single random-mating population with a finite and constant population size in an organism with nonoverlapping generations. This paper summarizes simulation studies of random genetic drift and selection in malaria parasites that take into account their unusual life history. Our results show that random genetic drift in the malaria life cycle is more pronounced than under the WF model. Paradoxically, the efficiency of purifying selection in the malaria life cycle is also greater than under WF, and the relative efficiency of positive selection varies according to conditions. Additionally, the site-frequency spectrum under neutrality is also more skewed toward low-frequency alleles than expected with WF. These results highlight the importance of considering the malaria life cycle when applying existing population genetic tools based on the WF model. The same caveat applies to other species with similarly complex life cycles. |
| doi_str_mv | 10.1073/pnas.1319857110 |
| format | Article |
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This proportion is much greater than observed in other organisms. Also unusual is that the site-frequency spectra of synonymous and non-synonymous polymorphisms are virtually indistinguishable. We hypothesized that the complicated life cycle of malaria parasites might lead to qualitatively different population genetics from that predicted from the classical Wright-Fisher (WF) model, which assumes a single random-mating population with a finite and constant population size in an organism with nonoverlapping generations. This paper summarizes simulation studies of random genetic drift and selection in malaria parasites that take into account their unusual life history. Our results show that random genetic drift in the malaria life cycle is more pronounced than under the WF model. Paradoxically, the efficiency of purifying selection in the malaria life cycle is also greater than under WF, and the relative efficiency of positive selection varies according to conditions. Additionally, the site-frequency spectrum under neutrality is also more skewed toward low-frequency alleles than expected with WF. These results highlight the importance of considering the malaria life cycle when applying existing population genetic tools based on the WF model. The same caveat applies to other species with similarly complex life cycles.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1319857110</identifier><identifier>PMID: 24259712</identifier><language>eng</language><publisher>United States: NATIONAL ACADEMY OF SCIENCES</publisher><subject>Alleles ; Biological Sciences ; Computer Simulation ; Evolutionary biology ; Founder Effect ; Gene Frequency ; Genetic Drift ; Genetic mutation ; Genetics, Population ; Life cycles ; life history ; Malaria ; Modeling ; Models, Genetic ; Mosquitos ; natural selection ; nucleotide sequences ; Parasite hosts ; Parasites ; Parasitic protozoa ; Plasmodium falciparum ; Plasmodium falciparum - genetics ; Plasmodium falciparum - physiology ; Polymorphism ; Polymorphism, Single Nucleotide - genetics ; Population genetics ; Population size ; random mating ; Selection, Genetic ; Senegal ; sequence analysis</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-12, Vol.110 (50), p.20129-20134</ispartof><rights>copyright © 1993–2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Dec 10, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c600t-2217627d0b762ea8bfd38397fa6d679bd51d7aae92ff0901ebc8349d6b7724cc3</citedby><cites>FETCH-LOGICAL-c600t-2217627d0b762ea8bfd38397fa6d679bd51d7aae92ff0901ebc8349d6b7724cc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/50.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23758122$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23758122$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24259712$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chang, Hsiao-Han</creatorcontrib><creatorcontrib>Moss, Eli L.</creatorcontrib><creatorcontrib>Park, Daniel J.</creatorcontrib><creatorcontrib>Ndiaye, Daouda</creatorcontrib><creatorcontrib>Mboup, Souleymane</creatorcontrib><creatorcontrib>Volkman, Sarah K.</creatorcontrib><creatorcontrib>Sabeti, Pardis C.</creatorcontrib><creatorcontrib>Wirth, Dyann F.</creatorcontrib><creatorcontrib>Neafsey, Daniel E.</creatorcontrib><creatorcontrib>Hartl, Daniel L.</creatorcontrib><title>Malaria life cycle intensifies both natural selection and random genetic drift</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Analysis of genome sequences of 159 isolates of Plasmodium falciparum from Senegal yields an extraordinarily high proportion (26.85%) of protein-coding genes with the ratio of nonsynonymous to synonymous polymorphism greater than one. This proportion is much greater than observed in other organisms. Also unusual is that the site-frequency spectra of synonymous and non-synonymous polymorphisms are virtually indistinguishable. We hypothesized that the complicated life cycle of malaria parasites might lead to qualitatively different population genetics from that predicted from the classical Wright-Fisher (WF) model, which assumes a single random-mating population with a finite and constant population size in an organism with nonoverlapping generations. This paper summarizes simulation studies of random genetic drift and selection in malaria parasites that take into account their unusual life history. Our results show that random genetic drift in the malaria life cycle is more pronounced than under the WF model. Paradoxically, the efficiency of purifying selection in the malaria life cycle is also greater than under WF, and the relative efficiency of positive selection varies according to conditions. Additionally, the site-frequency spectrum under neutrality is also more skewed toward low-frequency alleles than expected with WF. These results highlight the importance of considering the malaria life cycle when applying existing population genetic tools based on the WF model. The same caveat applies to other species with similarly complex life cycles.</description><subject>Alleles</subject><subject>Biological Sciences</subject><subject>Computer Simulation</subject><subject>Evolutionary biology</subject><subject>Founder Effect</subject><subject>Gene Frequency</subject><subject>Genetic Drift</subject><subject>Genetic mutation</subject><subject>Genetics, Population</subject><subject>Life cycles</subject><subject>life history</subject><subject>Malaria</subject><subject>Modeling</subject><subject>Models, Genetic</subject><subject>Mosquitos</subject><subject>natural selection</subject><subject>nucleotide sequences</subject><subject>Parasite hosts</subject><subject>Parasites</subject><subject>Parasitic protozoa</subject><subject>Plasmodium falciparum</subject><subject>Plasmodium falciparum - genetics</subject><subject>Plasmodium falciparum - physiology</subject><subject>Polymorphism</subject><subject>Polymorphism, Single Nucleotide - genetics</subject><subject>Population genetics</subject><subject>Population size</subject><subject>random mating</subject><subject>Selection, Genetic</subject><subject>Senegal</subject><subject>sequence analysis</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkjtvFDEQgC0EIkegpgJZoklzyfixfjRIUUQAKUADteX1ehOf9uzD9iLl3-PVHReggcZT-JvPM-NB6CWBcwKSXeyiLeeEEa06SQg8QisCmqwF1_AYrQCoXCtO-Ql6VsoGAHSn4Ck6oZx2WhK6Qp8_2cnmYPEURo_dvZs8DrH6WMIYfMF9qnc42jpnO-HiJ-9qSBHbOODcjrTFtz76Ghwechjrc_RktFPxLw7xFH27fvf16sP65sv7j1eXN2snAOqaUiIFlQP0LXir-nFgimk5WjEIqfuhI4O01ms6jqCB-N4pxvUgeikpd46dord7727ut35wPtZWoNnlsLX53iQbzJ83MdyZ2_TDMCU4A9IEZwdBTt9nX6rZhuL8NNno01wMUcAI6TRV_0a5poIo_j9WLqRgneh0Q9_8hW7SnGMbWqMkgBKaL29f7CmXUynZj8cWCZhlA8yyAeZhA1rG698nc-R_fXkD8AFYMo-65uvAUCB0qe3VHtmUmvKDgslOEUrZTyuTwBk</recordid><startdate>20131210</startdate><enddate>20131210</enddate><creator>Chang, Hsiao-Han</creator><creator>Moss, Eli L.</creator><creator>Park, Daniel J.</creator><creator>Ndiaye, Daouda</creator><creator>Mboup, Souleymane</creator><creator>Volkman, Sarah K.</creator><creator>Sabeti, Pardis C.</creator><creator>Wirth, Dyann F.</creator><creator>Neafsey, Daniel E.</creator><creator>Hartl, Daniel L.</creator><general>NATIONAL ACADEMY OF SCIENCES</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20131210</creationdate><title>Malaria life cycle intensifies both natural selection and random genetic drift</title><author>Chang, Hsiao-Han ; 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This proportion is much greater than observed in other organisms. Also unusual is that the site-frequency spectra of synonymous and non-synonymous polymorphisms are virtually indistinguishable. We hypothesized that the complicated life cycle of malaria parasites might lead to qualitatively different population genetics from that predicted from the classical Wright-Fisher (WF) model, which assumes a single random-mating population with a finite and constant population size in an organism with nonoverlapping generations. This paper summarizes simulation studies of random genetic drift and selection in malaria parasites that take into account their unusual life history. Our results show that random genetic drift in the malaria life cycle is more pronounced than under the WF model. Paradoxically, the efficiency of purifying selection in the malaria life cycle is also greater than under WF, and the relative efficiency of positive selection varies according to conditions. Additionally, the site-frequency spectrum under neutrality is also more skewed toward low-frequency alleles than expected with WF. These results highlight the importance of considering the malaria life cycle when applying existing population genetic tools based on the WF model. The same caveat applies to other species with similarly complex life cycles.</abstract><cop>United States</cop><pub>NATIONAL ACADEMY OF SCIENCES</pub><pmid>24259712</pmid><doi>10.1073/pnas.1319857110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Alleles Biological Sciences Computer Simulation Evolutionary biology Founder Effect Gene Frequency Genetic Drift Genetic mutation Genetics, Population Life cycles life history Malaria Modeling Models, Genetic Mosquitos natural selection nucleotide sequences Parasite hosts Parasites Parasitic protozoa Plasmodium falciparum Plasmodium falciparum - genetics Plasmodium falciparum - physiology Polymorphism Polymorphism, Single Nucleotide - genetics Population genetics Population size random mating Selection, Genetic Senegal sequence analysis |
| title | Malaria life cycle intensifies both natural selection and random genetic drift |
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