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Curr Biol. 2018 Oct 8;28(19):3193-3197.e5. doi: 10.1016/j.cub.2018.08.050. Epub 2018 Sep 27.

Reproductive Longevity Predicts Mutation Rates in Primates.

Author information

1
Department of Biology, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA; Department of Computer Science, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA. Electronic address: grthomas@indiana.edu.
2
Department of Biology, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA.
3
Department of Computer Science, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA.
4
Human Genome Sequencing Center, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
5
Keeling Center for Comparative Medicine and Research, University of Texas, MD Anderson Cancer Center, 650 Cool Water Drive, Bastrop, TX 78602, USA.
6
Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, 201 Dowman Drive, Atlanta, GA, USA; Division of Infectious Diseases, Department of Medicine, Emory University, 201 Dowman Drive, Atlanta, GA, USA.
7
Department of Biology, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA; Department of Computer Science, Indiana University, 107 S. Indiana Avenue, Bloomington, IN 47405, USA. Electronic address: mwh@indiana.edu.

Abstract

Mutation rates vary between species across several orders of magnitude, with larger organisms having the highest per-generation mutation rates. Hypotheses for this pattern typically invoke physiological or population-genetic constraints imposed on the molecular machinery preventing mutations [1]. However, continuing germline cell division in multicellular eukaryotes means that organisms with longer generation times and of larger size will leave more mutations to their offspring simply as a byproduct of their increased lifespan [2, 3]. Here, we deeply sequence the genomes of 30 owl monkeys (Aotus nancymaae) from six multi-generation pedigrees to demonstrate that paternal age is the major factor determining the number of de novo mutations in this species. We find that owl monkeys have an average mutation rate of 0.81 × 10-8 per site per generation, roughly 32% lower than the estimate in humans. Based on a simple model of reproductive longevity that does not require any changes to the mutational machinery, we show that this is the expected mutation rate in owl monkeys. We further demonstrate that our model predicts species-specific mutation rates in other primates, including study-specific mutation rates in humans based on the average paternal age. Our results suggest that variation in life history traits alone can explain variation in the per-generation mutation rate among primates, and perhaps among a wide range of multicellular organisms.

KEYWORDS:

de novo mutations; mutation rate; owl monkey; pedigree; reproductive longevity

PMID:
30270182
PMCID:
PMC6177314
[Available on 2019-10-08]
DOI:
10.1016/j.cub.2018.08.050

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