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Research Article

A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years

Priya Moorjani, Sriram Sankararaman, Qiaomei Fu, Molly Przeworski, Nick Patterson, and David Reich
  1. aDepartment of Biological Sciences, Columbia University, New York, NY 10027;
  2. bProgram in Medical and Population Genetics, Broad Institute, Cambridge, MA 02142;
  3. cDepartment of Genetics, Harvard Medical School, Boston, MA 02115;
  4. dDepartment of Computer Science, University of California, Los Angeles, CA 90095;
  5. eDepartment of Human Genetics, University of California, Los Angeles, CA 90095;
  6. fKey Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China;
  7. gDepartment of Systems Biology, Columbia University, New York, NY 10027;
  8. hHoward Hughes Medical Institute, Harvard Medical School, Boston, MA 02115

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PNAS May 17, 2016 113 (20) 5652-5657; first published May 2, 2016; https://doi.org/10.1073/pnas.1514696113
Priya Moorjani
aDepartment of Biological Sciences, Columbia University, New York, NY 10027;
bProgram in Medical and Population Genetics, Broad Institute, Cambridge, MA 02142;
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  • For correspondence: pm2730@columbia.edu reich@genetics.med.harvard.edu
Sriram Sankararaman
cDepartment of Genetics, Harvard Medical School, Boston, MA 02115;
dDepartment of Computer Science, University of California, Los Angeles, CA 90095;
eDepartment of Human Genetics, University of California, Los Angeles, CA 90095;
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Qiaomei Fu
cDepartment of Genetics, Harvard Medical School, Boston, MA 02115;
fKey Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China;
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Molly Przeworski
aDepartment of Biological Sciences, Columbia University, New York, NY 10027;
gDepartment of Systems Biology, Columbia University, New York, NY 10027;
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Nick Patterson
bProgram in Medical and Population Genetics, Broad Institute, Cambridge, MA 02142;
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David Reich
bProgram in Medical and Population Genetics, Broad Institute, Cambridge, MA 02142;
cDepartment of Genetics, Harvard Medical School, Boston, MA 02115;
hHoward Hughes Medical Institute, Harvard Medical School, Boston, MA 02115
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  • For correspondence: pm2730@columbia.edu reich@genetics.med.harvard.edu
  1. Edited by Andrew G. Clark, Cornell University, Ithaca, NY, and approved March 31, 2016 (received for review July 25, 2015)

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Significance

We report a method for dating ancient human samples that uses the recombination clock. To infer the age of ancient genomes, we take advantage of the shared history of Neanderthal gene flow into non-Africans that occurred around 50,000 y ago and measure the amount of “missing evolution” in terms of recombination breakpoints in the ancient genome compared with present-day samples. We show that this method provides age estimates that are highly correlated to radiocarbon dates, thus documenting the promise of this approach. By studying the linear relationship between the dates of Neanderthal admixture and the radiocarbon dates, we obtain, to our knowledge, the first direct estimate of the historical generation interval of 26–30 y.

Abstract

The study of human evolution has been revolutionized by inferences from ancient DNA analyses. Key to these studies is the reliable estimation of the age of ancient specimens. High-resolution age estimates can often be obtained using radiocarbon dating, and, while precise and powerful, this method has some biases, making it of interest to directly use genetic data to infer a date for samples that have been sequenced. Here, we report a genetic method that uses the recombination clock. The idea is that an ancient genome has evolved less than the genomes of present-day individuals and thus has experienced fewer recombination events since the common ancestor. To implement this idea, we take advantage of the insight that all non-Africans have a common heritage of Neanderthal gene flow into their ancestors. Thus, we can estimate the date since Neanderthal admixture for present-day and ancient samples simultaneously and use the difference as a direct estimate of the ancient specimen’s age. We apply our method to date five Upper Paleolithic Eurasian genomes with radiocarbon dates between 12,000 and 45,000 y ago and show an excellent correlation of the genetic and 14C dates. By considering the slope of the correlation between the genetic dates, which are in units of generations, and the 14C dates, which are in units of years, we infer that the mean generation interval in humans over this period has been 26–30 y. Extensions of this methodology that use older shared events may be applicable for dating beyond the radiocarbon frontier.

  • molecular clock
  • generation interval
  • ancient DNA
  • branch shortening

Footnotes

  • ↵1To whom correspondence may be addressed. Email: pm2730{at}columbia.edu or reich{at}genetics.med.harvard.edu.
  • Author contributions: P.M., N.P., and D.R. designed research; P.M., S.S., Q.F., M.P., N.P., and D.R. performed research; P.M. and S.S. contributed new reagents/analytic tools; P.M. and Q.F. analyzed data; and P.M., M.P., and D.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1514696113/-/DCSupplemental.

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Dating ancient genomes using a recombination clock
Priya Moorjani, Sriram Sankararaman, Qiaomei Fu, Molly Przeworski, Nick Patterson, David Reich
Proceedings of the National Academy of Sciences May 2016, 113 (20) 5652-5657; DOI: 10.1073/pnas.1514696113

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Dating ancient genomes using a recombination clock
Priya Moorjani, Sriram Sankararaman, Qiaomei Fu, Molly Przeworski, Nick Patterson, David Reich
Proceedings of the National Academy of Sciences May 2016, 113 (20) 5652-5657; DOI: 10.1073/pnas.1514696113
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Proceedings of the National Academy of Sciences: 113 (20)
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