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Population History and Natural Selection Shape Patterns of Genetic Variation in 132 Genes

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  • Joshua M Akey
  • Michael A Eberle
  • Mark J Rieder
  • Christopher S Carlson
  • Mark D Shriver
  • Deborah A Nickerson
  • Leonid Kruglyak

Abstract

Identifying regions of the human genome that have been targets of natural selection will provide important insights into human evolutionary history and may facilitate the identification of complex disease genes. Although the signature that natural selection imparts on DNA sequence variation is difficult to disentangle from the effects of neutral processes such as population demographic history, selective and demographic forces can be distinguished by analyzing multiple loci dispersed throughout the genome. We studied the molecular evolution of 132 genes by comprehensively resequencing them in 24 African-Americans and 23 European-Americans. We developed a rigorous computational approach for taking into account multiple hypothesis tests and demographic history and found that while many apparent selective events can instead be explained by demography, there is also strong evidence for positive or balancing selection at eight genes in the European-American population, but none in the African-American population. Our results suggest that the migration of modern humans out of Africa into new environments was accompanied by genetic adaptations to emergent selective forces. In addition, a region containing four contiguous genes on Chromosome 7 showed striking evidence of a recent selective sweep in European-Americans. More generally, our results have important implications for mapping genes underlying complex human diseases. An analysis of 132 human genes suggests that the migration of modern humans out of Africa into new environments was accompanied by genetic adaptations to emergent selective forces.

Suggested Citation

  • Joshua M Akey & Michael A Eberle & Mark J Rieder & Christopher S Carlson & Mark D Shriver & Deborah A Nickerson & Leonid Kruglyak, 2004. "Population History and Natural Selection Shape Patterns of Genetic Variation in 132 Genes," PLOS Biology, Public Library of Science, vol. 2(10), pages 1-1, September.
  • Handle: RePEc:plo:pbio00:0020286
    DOI: 10.1371/journal.pbio.0020286
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    Cited by:

    1. Magnus Nordborg & Tina T Hu & Yoko Ishino & Jinal Jhaveri & Christopher Toomajian & Honggang Zheng & Erica Bakker & Peter Calabrese & Jean Gladstone & Rana Goyal & Mattias Jakobsson & Sung Kim & Yuri , 2005. "The Pattern of Polymorphism in Arabidopsis thaliana," PLOS Biology, Public Library of Science, vol. 3(7), pages 1-1, May.
    2. Rafajlović, M. & Klassmann, A. & Eriksson, A. & Wiehe, T. & Mehlig, B., 2014. "Demography-adjusted tests of neutrality based on genome-wide SNP data," Theoretical Population Biology, Elsevier, vol. 95(C), pages 1-12.
    3. Pleuni S Pennings & Joachim Hermisson, 2006. "Soft Sweeps III: The Signature of Positive Selection from Recurrent Mutation," PLOS Genetics, Public Library of Science, vol. 2(12), pages 1-15, December.
    4. Pei-Kuan Cong & Wei-Yang Bai & Jin-Chen Li & Meng-Yuan Yang & Saber Khederzadeh & Si-Rui Gai & Nan Li & Yu-Heng Liu & Shi-Hui Yu & Wei-Wei Zhao & Jun-Quan Liu & Yi Sun & Xiao-Wei Zhu & Pian-Pian Zhao , 2022. "Genomic analyses of 10,376 individuals in the Westlake BioBank for Chinese (WBBC) pilot project," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Ryosuke Kimura & Akihiro Fujimoto & Katsushi Tokunaga & Jun Ohashi, 2007. "A Practical Genome Scan for Population-Specific Strong Selective Sweeps That Have Reached Fixation," PLOS ONE, Public Library of Science, vol. 2(3), pages 1-10, March.
    6. Terence C. Burnham & Aimee Dunlap & David W. Stephens, 2015. "Experimental Evolution and Economics," SAGE Open, , vol. 5(4), pages 21582440156, November.

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