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Variation in the molecular clock of primates

Priya Moorjani, Carlos Eduardo G. Amorim, Peter F. Arndt, Molly Przeworski
doi: https://doi.org/10.1101/036434
Priya Moorjani
1Department of Biological Sciences, Columbia University, New York, NY
2Program in Medical and Population Genetics, Broad Institute, Cambridge, MA
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  • For correspondence: pm2730@columbia.edu mp3284@columbia.edu
Carlos Eduardo G. Amorim
1Department of Biological Sciences, Columbia University, New York, NY
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Peter F. Arndt
3Max Planck Institute for Molecular Genetics, Berlin, Germany
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Molly Przeworski
1Department of Biological Sciences, Columbia University, New York, NY
4Dept. of Systems Biology, Columbia University, New York, NY
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  • For correspondence: pm2730@columbia.edu mp3284@columbia.edu
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Abstract

Events in primate evolution are often dated by assuming a “molecular clock”, i.e., a constant rate of substitution per unit time, but the validity of this assumption remains unclear. Among mammals, it is well known that there exists substantial variation in yearly substitution rates. Such variation is to be expected from differences in life-history traits, suggesting that it should also be found among primates. Motivated by these considerations, we analyze whole genomes from ten primate species, including Old World Monkeys (OWMs), New World Monkeys (NWMs) and apes, focusing on putatively neutral autosomal sites and controlling for possible effects of biased gene conversion and methylation at CpG sites. We find that substitution rates are ˜65% higher in lineages leading from the hominoid-NWM ancestor to NWMs than to apes. Within apes, rates are ˜2% higher in chimpanzees and ˜7% higher in the gorilla than in humans. Substitution types subject to biased gene conversion show no more variation among species than those not subject to it. Not all mutation types behave similarly, however: in particular, transitions at CpG sites exhibit a more clock-like behavior than do other types, presumably due to their non-replicative origin. Thus, not only the total rate, but also the mutational spectrum varies among primates. This finding suggests that events in primate evolution are most reliably dated using CpG transitions. Taking this approach, we estimate that the average time to the most recent common ancestor of human and chimpanzee is 12.1 million years and their split time 7.9 million years.

Significance statement Much of our understanding of the chronology of human evolution relies on the “molecular clock”, i.e., a constant rate of substitutions per unit time. To evaluate the validity of this assumption, we analyze whole genome sequences from ten primate species. We find that there is substantial variation in the molecular clock between apes and monkeys, and rates even differ within hominoids. Importantly, not all mutation types behave similarly: notably, transitions at CpG sites exhibit a more clock-like behavior than other substitutions, presumably due to their non-replicative origin. Thus, the mutation spectra, and not just the overall substitution rates, are changing across primates. This finding further suggests that events in primate evolution are most reliably dated using CpG transitions.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 11, 2016.
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Variation in the molecular clock of primates
Priya Moorjani, Carlos Eduardo G. Amorim, Peter F. Arndt, Molly Przeworski
bioRxiv 036434; doi: https://doi.org/10.1101/036434
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Variation in the molecular clock of primates
Priya Moorjani, Carlos Eduardo G. Amorim, Peter F. Arndt, Molly Przeworski
bioRxiv 036434; doi: https://doi.org/10.1101/036434

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