Distance from sub-Saharan Africa predicts mutational load in diverse human genomes
The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 4; pp. E440 - E449 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
26.01.2016
National Acad Sciences |
| Series | From the Cover |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 |
| DOI | 10.1073/pnas.1510805112 |
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| Abstract | The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive. |
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| AbstractList | The Out-of-Africa (OOA) dispersal ~50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive. Human genomes carry hundreds of mutations that are predicted to be deleterious in some environments, potentially affecting the health or fitness of an individual. We characterize the distribution of deleterious mutations among diverse human populations, modeled under different selection coefficients and dominance parameters. Using a new dataset of diverse human genomes from seven different populations, we use spatially explicit simulations to reveal that classes of deleterious alleles have very different patterns across populations, reflecting the interaction between genetic drift and purifying selection. We show that there is a strong signal of purifying selection at conserved genomic positions within African populations, but most predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive. The Out-of-Africa (OOA) dispersal ∼ 50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive. The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population genetics theory predicts an increase of mutational load in populations undergoing serial founder effects during range expansions. To test this hypothesis, we have sequenced full genomes and high-coverage exomes from seven geographically divergent human populations from Namibia, Congo, Algeria, Pakistan, Cambodia, Siberia, and Mexico. We find that individual genomes vary modestly in the overall number of predicted deleterious alleles. We show via spatially explicit simulations that the observed distribution of deleterious allele frequencies is consistent with the OOA dispersal, particularly under a model where deleterious mutations are recessive. We conclude that there is a strong signal of purifying selection at conserved genomic positions within Africa, but that many predicted deleterious mutations have evolved as if they were neutral during the expansion out of Africa. Under a model where selection is inversely related to dominance, we show that OOA populations are likely to have a higher mutation load due to increased allele frequencies of nearly neutral variants that are recessive or partially recessive. |
| Author | Henn, Brenna M. Botigué, Laura R. Martin, Alicia R. Musharoff, Shaila Excoffier, Laurent Snyder, Michael P. Lipatov, Mikhail Kidd, Jeffrey M. Maples, Brian K. Peischl, Stephan Cann, Howard Bustamante, Carlos D. Dupanloup, Isabelle |
| Author_xml | – sequence: 1 givenname: Brenna M. surname: Henn fullname: Henn, Brenna M. organization: Department of Ecology and Evolution, Stony Brook University, The State University of New York, Stony Brook, NY 11794 – sequence: 2 givenname: Laura R. surname: Botigué fullname: Botigué, Laura R. organization: Department of Ecology and Evolution, Stony Brook University, The State University of New York, Stony Brook, NY 11794 – sequence: 3 givenname: Stephan surname: Peischl fullname: Peischl, Stephan organization: Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland – sequence: 4 givenname: Isabelle surname: Dupanloup fullname: Dupanloup, Isabelle organization: Institute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland – sequence: 5 givenname: Mikhail surname: Lipatov fullname: Lipatov, Mikhail organization: Department of Ecology and Evolution, Stony Brook University, The State University of New York, Stony Brook, NY 11794 – sequence: 6 givenname: Brian K. surname: Maples fullname: Maples, Brian K. organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305 – sequence: 7 givenname: Alicia R. surname: Martin fullname: Martin, Alicia R. organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305 – sequence: 8 givenname: Shaila surname: Musharoff fullname: Musharoff, Shaila organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305 – sequence: 9 givenname: Howard surname: Cann fullname: Cann, Howard organization: Centre d’Etude du Polymorphisme Humain, Foundation Jean Dausset, 75010 Paris, France – sequence: 10 givenname: Michael P. surname: Snyder fullname: Snyder, Michael P. organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305 – sequence: 11 givenname: Laurent surname: Excoffier fullname: Excoffier, Laurent organization: Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland – sequence: 12 givenname: Jeffrey M. surname: Kidd fullname: Kidd, Jeffrey M. organization: Department of Human Genetics and Department of Computational Medicine and Bioinformatics, University of Michigan Medical School, Ann Arbor, MI 48109 – sequence: 13 givenname: Carlos D. surname: Bustamante fullname: Bustamante, Carlos D. organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26712023$$D View this record in MEDLINE/PubMed |
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| Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Jan 26, 2016 |
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| Keywords | mutation purifying selection range expansion expansion load founder effect |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-2 content type line 23 ObjectType-Article-1 ObjectType-Feature-2 Author contributions: B.M.H., M.P.S., L.E., J.M.K., and C.D.B. designed research; B.M.H., L.R.B., S.P., and J.M.K. performed research; S.P., H.C., and L.E. contributed new reagents/analytic tools; B.M.H., L.R.B., S.P., I.D., M.L., B.K.M., A.R.M., S.M., and J.M.K. analyzed data; and B.M.H., L.R.B., S.P., L.E., J.M.K., and C.D.B. wrote the paper. Edited by Charles F. Aquadro, Cornell University, Ithaca, NY, and accepted by the Editorial Board November 13, 2015 (received for review June 9, 2015) 1B.M.H., L.R.B., and S.P. contributed equally to this work. 4L.E., J.M.K., and C.D.B. contributed equally to this work. |
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| PublicationDate_xml | – month: 01 year: 2016 text: 2016-01-26 day: 26 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: Washington |
| PublicationSeriesTitle | From the Cover |
| PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
| PublicationTitleAlternate | Proc Natl Acad Sci U S A |
| PublicationYear | 2016 |
| Publisher | National Academy of Sciences National Acad Sciences |
| Publisher_xml | – name: National Academy of Sciences – name: National Acad Sciences |
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| Snippet | The Out-of-Africa (OOA) dispersal ∼50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population... Human genomes carry hundreds of mutations that are predicted to be deleterious in some environments, potentially affecting the health or fitness of an... The Out-of-Africa (OOA) dispersal ∼ 50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population... The Out-of-Africa (OOA) dispersal ~50,000 y ago is characterized by a series of founder events as modern humans expanded into multiple continents. Population... |
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| SubjectTerms | Africa South of the Sahara African Continental Ancestry Group - genetics Alleles Animals Asian Continental Ancestry Group - genetics Biological Sciences Computer Simulation Conserved Sequence Dispersal Ethnic Groups - genetics Evolution, Molecular Founder Effect Gene Flow Genetic Diseases, Inborn - genetics Genetic Drift Genetics Genome, Human Genomes Genomics Genotype Homing Behavior Human Migration Human populations Humans Indians, Central American - genetics Models, Genetic Mutation PNAS Plus Population genetics Selection, Genetic |
| Title | Distance from sub-Saharan Africa predicts mutational load in diverse human genomes |
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