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Direct estimation of mutations in great apes reconciles phylogenetic dating
Abstract
The human mutation rate per generation estimated from trio sequencing has revealed an almost linear relationship with the age of the father and the age of the mother, with fathers contributing about three times as many mutations per year as mothers. The yearly trio-based mutation rate estimate of around 0.43 × 10-9 is markedly lower than previous indirect estimates of about 1 × 10-9 per year from phylogenetic comparisons of the great apes calibrated by fossil evidence. This suggests either a slowdown in the accumulation of mutations per year in the human lineage over the past 10 million years or an inaccurate interpretation of the fossil record. Here we inferred de novo mutations in chimpanzee, gorilla, and orangutan parent-offspring trios. Extrapolating the relationship between the mutation rate and the age of parents from humans to these other great apes, we estimated that each species has higher mutation rates per year by factors of 1.50 ± 0.10, 1.51 ± 0.23, and 1.42 ± 0.22 for chimpanzee, gorilla, and orangutan, respectively, and by a factor of 1.48 ± 0.08 for the three species combined. These estimates suggest an appreciable slowdown in the yearly mutation rate in the human lineage that is likely to be recent as genome comparisons almost adhere to a molecular clock. If the nonhuman rates rather than the human rate are extrapolated over the phylogeny of the great apes, we estimate divergence and speciation times that are much more in line with the fossil record and the biogeography.
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“The similar mutation rates in Neanderthals and modern humans imply that the apparent slowdown in the human mutation rate 36 is unlikely to have occurred between 500,000 and 55,000 years ago.”
From The nature of Neanderthal introgression revealed by 27,566 Icelandic genomes (2020) · cites this paper as [36]
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Cites
Rate of de novo mutations and the importance of father’s age to disease risk
Kong, A., Frigge, M. L., Masson, G., Besenbacher, S., Sulem, P., Magnusson, G., Gudjonsson, S. A., Sigurdsson, A., Jonasdottir, A., Jonasdottir, A., et al. (2012) · Nature · doi:10.1038/nature11396 · Cited by 2,134
Self-citationInsights into hominid evolution from the gorilla genome sequence
Scally, A., Dutheil, J. Y., Hillier, L. W., Jordan, G. E., Goodhead, I., Herrero, J., Hobolth, A., Lappalainen, T., Mailund, T., Marquès‐Bonet, T., et al. (2012) · Nature · doi:10.1038/nature10842 · Cited by 776
Self-citationA high-coverage Neandertal genome from Vindija Cave in Croatia
Prüfer, K., de Filippo, C., Grote, S., Mafessoni, F., Korlević, P., Hajdinjak, M., Vernot, B., Skov, L., Hsieh, P., Peyrégne, S., et al. (2017) · Science · doi:10.1126/science.aao1887 · Cited by 719
Self-citationArdipithecus ramidus and the Paleobiology of Early Hominids
White, T. D., Asfaw, B., Beyene, Y., Haile‐Selassie, Y., Lovejoy, C. O., Suwa, G., & WoldeGabriel, G. (2009) · Science · doi:10.1126/science.1175802 · Cited by 693
Revising the human mutation rate: implications for understanding human evolution
Scally, A., & Durbin, R. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3295 · Cited by 610
Parental influence on human germline de novo mutations in 1,548 trios from Iceland
Jónsson, H., Sulem, P., Kehr, B., Kristmundsdottir, S., Zink, F., Hjartarson, E., Hardarson, M. T., Hjorleifsson, K. E., Eggertsson, H. P., Gudjonsson, S. A., et al. (2017) · Nature · doi:10.1038/nature24018 · Cited by 561
Orrorin tugenensis Femoral Morphology and the Evolution of Hominin Bipedalism
Richmond, B. G., & Jungers, W. L. (2008) · Science · doi:10.1126/science.1154197 · Cited by 278
Variation in the molecular clock of primates
Moorjani, P., Amorim, C. E. G., Arndt, P. F., & Przeworski, M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600374113 · Cited by 248
Overlooked roles of DNA damage and maternal age in generating human germline mutations
Gao, Z., Moorjani, P., Sasani, T. A., Pedersen, B. S., Quinlan, A. R., Jorde, L. B., Amster, G., & Przeworski, M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901259116 · Cited by 229
Moorjani, P., Sankararaman, S., Fu, Q., Przeworski, M., Patterson, N., & Reich, D. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514696113 · Cited by 174
Novel variation and de novo mutation rates in population-wide de novo assembled Danish trios
Besenbacher, S., Liu, S. M., Izarzugaza, J. M. G., Grove, J., Belling, K., Bork‐Jensen, J., Huang, S., Als, T. D., Li, S., Yadav, R., et al. (2015) · Nature Communications · doi:10.1038/ncomms6969 · Cited by 169
Self-citationNew Sivapithecus humeri from Pakistan and the relationship of Sivapithecus and Pongo
Pilbeam, D. R., Rose, M. D., Barry, J. C., & Shah, S. M. I. (1990) · Nature · doi:10.1038/348237a0 · Cited by 161
Strong male bias drives germline mutation in chimpanzees
Venn, O., Turner, I., Mathieson, I., de Groot, N., Bontrop, R. E., & McVean, G. (2014) · Science · doi:10.1126/science.344.6189.1272 · Cited by 158
Sequencing and de novo assembly of 150 genomes from Denmark as a population reference
Maretty, L., Jensen, J. M., Petersen, B., Sibbesen, J. A., Liu, S. M., Villesen, P., Skov, L., Belling, K., Have, C. T., Izarzugaza, J. M. G., et al. (2017) · Nature · doi:10.1038/nature23264 · Cited by 151
Self-citationThe mutation rate in human evolution and demographic inference
Scally, A. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.07.008 · Cited by 145
Life history effects on the molecular clock of autosomes and sex chromosomes
Amster, G., & Sella, G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515798113 · Cited by 134
Multiple transmissions of de novo mutations in families
Jónsson, H., Sulem, P., Arnadottir, G. A., Pálsson, G., Eggertsson, H. P., Kristmundsdóttir, S., Zink, F., Kehr, B., Hjörleifsson, K. E., Jensson, B. Ö., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0259-9 · Cited by 115
Reproductive Longevity Predicts Mutation Rates in Primates
Thomas, G. W. C., Wang, R. J., Puri, A., Harris, R. A., Raveendran, M., Hughes, D., Murali, S. C., Williams, L. E., Doddapaneni, H., Muzny, D. M., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.050 · Cited by 103
Goldmann, J. M., Seplyarskiy, V. B., Wong, W. S. W., Vilboux, T., Neerincx, P. B. T., Bodian, D. L., Solomon, B. D., Veltman, J. A., Deeken, J. F., Gilissen, C., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0071-6 · Cited by 89
Human Germline Mutation and the Erratic Evolutionary Clock
Moorjani, P., Gao, Z., & Przeworski, M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.2000744 · Cited by 68
Calibrating the Human Mutation Rate via Ancestral Recombination Density in Diploid Genomes
Lipson, M., Loh, P., Sankararaman, S., Patterson, N. J., Berger, B., & Reich, D. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005550 · Cited by 65
Mutation rates and the evolution of germline structure
Scally, A. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0137 · Cited by 58
Tatsumoto, S., Go, Y., Fukuta, K., Noguchi, H., Hayakawa, T., Tomonaga, M., Hirai, H., Matsuzawa, T., Agata, K., & Fujiyama, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-13919-7 · Cited by 47
ASGART: fast and parallel genome scale segmental duplications mapping
Delehelle, F., Cussat‐Blanc, S., Alliot, J., Luga, H., & Balaresque, P. L. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty172 · Cited by 27
Research works printed but not linked: 1
- Lindsay, S. J., Rahbari, R., Kaplanis, J., Keane, T. & Hurles, M. Striking differences in patterns of germline mutation between mice and humans. Preprint at https://www.biorxiv.org/content/early/2018/05/23/082297 (2018).
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“…estimates of long-term evolutionary rates are not necessarily applicable at the population level (Ho, Duchêne, Molak, & Shapiro, 2015); rates of spontaneous mutation have been inferred for a limited number of eukaryote species (Besenbacher et al., 2019; Smeds, Qvarnström, & Ellegren, 2016).”
Background
Metadata
- Authors
- Besenbacher, S., Hvilsom, C., Marques-Bonet, T., Mailund, T., & Schierup, M. H.
- Affiliations
- Aarhus University (DK)
- Copenhagen Zoo (DK)
- Corresponding author
- Besenbacher, Søren
- Schierup, Mikkel Heide
- Venue
- Nature Ecology & Evolution
- Published
- 2019-01-21
- Volume
- 3
- Issue
- 2
- Pages
- 286-292
- ISSN
- 2397-334X (ISSN-L)
- OpenAlex
- W2910586282
- Cited by
- 165
- References
- 24
- Citations by year
- 2026: 13 · 2025: 20 · 2024: 19 · 2023: 25 · 2022: 25 · 2021: 30 · 2020: 17 · 2019: 15
- FWCI
- 7.46
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-04-15)
- Open access
- closed
- Licence
- Locations
- Nature Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Scopus (Elsevier) (submittedVersion)
- Funders
- Novo Nordisk Fonden (NNF18OC0031004)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Anthropology › Pleistocene-Era Hominins and Archaeology
- Keywords
- mutation rate, de novo mutations, great apes, chimpanzees, gorillas, orangutans, parent-offspring trios, molecular clock, divergence time estimation, speciation time, fossil record, human lineage
- MeSH terms
- Animals, Biological Evolution, Fossils, Mutation, Phylogeny, Genetic Variation, Hominidae, Evolution, Molecular
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