Abstract
Establishing the age of each mutation segregating in contemporary human populations is important to fully understand our evolutionary history and will help to facilitate the development of new approaches for disease-gene discovery. Large-scale surveys of human genetic variation have reported signatures of recent explosive population growth, notable for an excess of rare genetic variants, suggesting that many mutations arose recently. To more quantitatively assess the distribution of mutation ages, we resequenced 15,336 genes in 6,515 individuals of European American and African American ancestry and inferred the age of 1,146,401 autosomal single nucleotide variants (SNVs). We estimate that approximately 73% of all protein-coding SNVs and approximately 86% of SNVs predicted to be deleterious arose in the past 5,000-10,000 years. The average age of deleterious SNVs varied significantly across molecular pathways, and disease genes contained a significantly higher proportion of recently arisen deleterious SNVs than other genes. Furthermore, European Americans had an excess of deleterious variants in essential and Mendelian disease genes compared to African Americans, consistent with weaker purifying selection due to the Out-of-Africa dispersal. Our results better delimit the historical details of human protein-coding variation, show the profound effect of recent human history on the burden of deleterious SNVs segregating in contemporary populations, and provide important practical information that can be used to prioritize variants in disease-gene discovery.
MeSH Terms
Africa/ethnology
Alleles
Blacks/genetics
Europe/ethnology
Evolution, Molecular
Exome/genetics
Exons/genetics
Genetic Variation/genetics
Humans
Open Reading Frames/genetics
Polymorphism, Single Nucleotide/genetics
United States
Whites/genetics
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Fu Wenqing
Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA.
[email protected]
O'Connor Timothy D
Jun Goo
Kang Hyun Min
Abecasis Goncalo
Leal Suzanne M
Gabriel Stacey
Rieder Mark J
Altshuler David
Shendure Jay
Nickerson Deborah A
Bamshad Michael J
NHLBI Exome Sequencing Project
Akey Joshua M
Investigators
396 investigators, click to expand
Gabriel Stacey B
Altshuler David M
Gonçalo R Abecasis
Allayee Hooman
Cresci Sharon
Daly Mark J
de Bakker Paul I W
DePristo Mark A
Do Ron
Donnelly Peter
Farlow Deborah N
Fennell Tim
Garimella Kiran
Hazen Stanley L
Hu Youna
Jordan Daniel M
Jun Goo
Kathiresan Sekar
Kang Hyun Min
Kiezun Adam
Lettre Guillaume
Li Bingshan
Li Mingyao
Newton-Cheh Christopher H
Padmanabhan Sandosh
Peloso Gina
Pulit Sara
Rader Daniel J
Reich David
Reilly Muredach P
Rivas Manuel A
Schwartz Steve
Hutchinson Fred
Scott Laura
Siscovick David S
Spertus John A
Stitziel Nathaniel O
Stoletzki Nina
Sunyaev Shamil R
Voight Benjamin F
Willer Cristen J
Rich Stephen S
Akylbekova Ermeg
Atwood Larry D
Ballantyne Christie M
Barbalic Maja
Barr R Graham
Benjamin Emelia J
Bis Joshua
Boerwinkle Eric
Bowden Donald W
Brody Jennifer
Budoff Matthew
Burke Greg
Buxbaum Sarah
Carr Jeff
Chen Donna T
Chen Ida Y
Chen Wei-Min
Concannon Pat
Crosby Jacy
Cupples L Adrienne
D'Agostino Ralph
DeStefano Anita L
Dreisbach Albert
Dupuis Josée
Durda J Peter
Ellis Jaclyn
Folsom Aaron R
Fornage Myriam
Fox Caroline S
Fox Ervin
Funari Vincent
Ganesh Santhi K
Gardin Julius
Goff David
Gordon Ora
Grody Wayne
Gross Myron
Guo Xiuqing
Hall Ira M
Heard-Costa Nancy L
Heckbert Susan R
Heintz Nicholas
Herrington David M
Hickson DeMarc
Huang Jie
Hwang Shih-Jen
Jacobs David R
Jenny Nancy S
Johnson Andrew D
Johnson Craig W
Kawut Steven
Kronmal Richard
Kurz Raluca
Lange Ethan M
Lange Leslie A
Larson Martin G
Lawson Mark
Lewis Cora E
Levy Daniel
Li Dalin
Lin Honghuang
Liu Chunyu
Liu Jiankang
Liu Kiang
Liu Xiaoming
Liu Yongmei
Longstreth William T
Loria Cay
Lumley Thomas
Lunetta Kathryn
Mackey Aaron J
Mackey Rachel
Manichaikul Ani
Maxwell Taylor
McKnight Barbara
Meigs James B
Morrison Alanna C
Musani Solomon K
Mychaleckyj Josyf C
Nettleton Jennifer A
North Kari
O'Donnell Christopher J
O'Leary Daniel
Ong Frank
Palmas Walter
Pankow James S
Pankratz Nathan D
Paul Shom
Perez Marco
Person Sharina D
Polak Joseph
Post Wendy S
Psaty Bruce M
Quinlan Aaron R
Raffel Leslie J
Ramachandran Vasan S
Reiner Alexander P
Rice Kenneth
Rotter Jerome I
Sanders Jill P
Schreiner Pamela
Seshadri Sudha
Shea Steve
Sidney Stephen
Silverstein Kevin
Siscovick David S
Smith Nicholas L
Sotoodehnia Nona
Srinivasan Asoke
Taylor Herman A
Taylor Kent
Thomas Fridtjof
Tracy Russell P
Tsai Michael Y
Volcik Kelly A
Wassel Chrstina L
Watson Karol
Wei Gina
White Wendy
Wiggins Kerri L
Wilk Jemma B
Williams O Dale
Wilson Gregory
Wilson James G
Wolf Phillip
Zakai Neil A
Hardy John
Meschia James F
Nalls Michael
Rich Stephen S
Singleton Andrew
Worrall Brad
Bamshad Michael J
Barnes Kathleen C
Abdulhamid Ibrahim
Accurso Frank
Anbar Ran
Beaty Terri
Bigham Abigail
Black Phillip
Bleecker Eugene
Buckingham Kati
Cairns Anne Marie
Chen Wei-Min
Caplan Daniel
Chatfield Barbara
Chidekel Aaron
Cho Michael
Christiani David C
Crapo James D
Crouch Julia
Daley Denise
Dang Anthony
Dang Hong
De Paula Alicia
DeCelie-Germana Joan
Dozor Allen
Drumm Mitch
Dyson Maynard
Emerson Julia
Emond Mary J
Ferkol Thomas
Fink Robert
Foster Cassandra
Froh Deborah
Gao Li
Gershan William
Gibson Ronald L
Godwin Elizabeth
Gondor Magdalen
Gutierrez Hector
Hansel Nadia N
Hassoun Paul M
Hiatt Peter
Hokanson John E
Howenstine Michelle
Hummer Laura K
Kanga Jamshed
Kim Yoonhee
Knowles Michael R
Konstan Michael
Lahiri Thomas
Laird Nan
Lange Christoph
Lin Lin
Lin Xihong
Louie Tin L
Lynch David
Make Barry
Martin Thomas R
Mathai Steve C
Mathias Rasika A
McNamara John
McNamara Sharon
Meyers Deborah
Millard Susan
Mogayzel Peter
Moss Richard
Murray Tanda
Nielson Dennis
Noyes Blakeslee
O'Neal Wanda
Orenstein David
O'Sullivan Brian
Pace Rhonda
Pare Peter
Parker H Worth
Passero Mary Ann
Perkett Elizabeth
Prestridge Adrienne
Rafaels Nicholas M
Ramsey Bonnie
Regan Elizabeth
Ren Clement
Retsch-Bogart George
Rock Michael
Rosen Antony
Rosenfeld Margaret
Ruczinski Ingo
Sanford Andrew
Schaeffer David
Sell Cindy
Sheehan Daniel
Silverman Edwin K
Sin Don
Spencer Terry
Stonebraker Jackie
Tabor Holly K
Varlotta Laurie
Vergara Candelaria I
Weiss Robert
Wigley Fred
Wise Robert A
Wright Fred A
Wurfel Mark M
Zanni Robert
Zou Fei
Nickerson Deborah A
Rieder Mark J
Green Phil
Shendure Jay
Akey Joshua M
Bamshad Michael J
Bustamante Carlos D
Crosslin David R
Eichler Evan E
Fox P Keolu
Fu Wenqing
Gordon Adam
Gravel Simon
Jarvik Gail P
Johnsen Jill M
Kan Mengyuan
Kenny Eimear E
Kidd Jeffrey M
Lara-Garduno Fremiet
Leal Suzanne M
Liu Dajiang J
McGee Sean
O'Connor Timothy D
Paeper Bryan
Robertson Peggy D
Smith Joshua D
Tennessen Jacob A
Turner Emily H
Wang Gao
Jackson Rebecca
North Kari
Peters Ulrike
Carlson Christopher S
Anderson Garnet
Anton-Culver Hoda
Assimes Themistocles L
Auer Paul L
Hutchinson Fred
Beresford Shirley
Hutchinson Fred
Bizon Chris
Black Henry
Brunner Robert
Brzyski Robert
Burwen Dale
Caan Bette
Carty Cara L
Chlebowski Rowan
Cummings Steven
Curb J David
Eaton Charles B
Ford Leslie
Franceschini Nora
Fullerton Stephanie M
Gass Margery
Geller Nancy
Heiss Gerardo
Howard Barbara V
Hsu Li
Hutter Carolyn M
Ioannidis John
Jiao Shuo
Johnson Karen C
Kooperberg Charles
Kuller Lewis
LaCroix Andrea
Lakshminarayan Kamakshi
Lane Dorothy
Lange Ethan M
Lange Leslie A
Lasser Norman
LeBlanc Erin
Lewis Cora E
Li Kuo-Ping
Limacher Marian
Lin Dan-Yu
Logsdon Benjamin A
Ludlam Shari
Manson JoAnn E
Margolis Karen
Martin Lisa
McGowan Joan
Monda Keri L
Kotchen Jane Morley
Nathan Lauren
Ockene Judith
O'Sullivan Mary Jo
Phillips Lawrence S
Prentice Ross L
Reiner Alexander P
Hutchinson Fred
Robbins John
Robinson Jennifer G
Rossouw Jacques E
Sangi-Haghpeykar Haleh
Sarto Gloria E
Shumaker Sally
Simon Michael S
Stefanick Marcia L
Stein Evan
Tang Hua
Taylor Kira C
Thomson Cynthia A
Thornton Timothy A
Van Horn Linda
Vitolins Mara
Wactawski-Wende Jean
Wallace Robert
Wassertheil-Smoller Sylvia
Zeng Donglin
Applebaum-Bowden Deborah
Feolo Michael
Gan Weiniu
Paltoo Dina N
Rossouw Jacques E
Sholinsky Phyliss
Sturcke Anne
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