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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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“…et al., 2015), or at least 2–2.5 million years (Antón et al., 2014; Kimbel & Villmoare, 2016), and the split between our earliest hominin ancestors and the genus Pan is most commonly traced to around 5–7 million years ago (Besenbacher et al., 2019; Car-roll, 2003; Langergraber et al., 2012).”
InfluentialJovanović, V., Sarfert, M., Reyna-Blanco, C. S., Indrischek, H., Valdivia, D. I., Shelest, E., & Nowick, K. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.662239 · Cited by 23
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“[1]) and accurate estimates of mutation rates within species or across the genome [2, 3, 4, 5].”
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“While some species have been studied for mutation rates using a limited number of trios [2–5], only humans [6, 7] and mice [8] have been studied with sufficient numbers of trios sequenced and analyzed to allow for intraspecific investigation of factors influencing mutation rates.”
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“using a single chimpanzee trio (previously published by several of the authors) is less useful in this regard, because (i) the previous study used a similarly high GQ threshold (≥65) [5] as their own pipeline (≥60) and (ii) previously identified de novo mutation candidates were not independently validated by an orthog…”
BackgroundAncient trans-species polymorphism at the Major Histocompatibility Complex in primates
Fortier, A. L., & Pritchard, J. K. (2025) · eLife · doi:10.7554/elife.103547.3 · Cited by 14
Thom, G., Moreira, L. R., Batista, R., Gehara, M., Aleixo, A. L. P., & Smith, B. T. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae002 · Cited by 15
“For instance, levels of polymorphism could be associated with variation in mutation rate (Jónsson et al. 2018; Smith et al. 2018; Besenbacher et al. 2019; Barroso and Dutheil 2021).”
BackgroundLocal genetic adaptation to habitat in wild chimpanzees
Ostridge, H. J., Fontsere, C., Lizano, E., Soto, D. C., Schmidt, J. M., Saxena, V., Álvarez-Estapé, M., Barratt, C. D., Gratton, P., Bocksberger, G., et al. (2025) · Science · doi:10.1126/science.adn7954 · Cited by 17
Rocks and clocks revised: New promises and challenges in dating the primate tree of life
Pozzi, L., & Penna, A. (2022) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21940 · Cited by 15
Great apes and humans evolved from a long-backed ancestor
Machnicki, A. L., & Reno, P. L. (2020) · Journal of Human Evolution · doi:10.1016/j.jhevol.2020.102791 · Cited by 14
Stability across the Whole Nuclear Genome in the Presence and Absence of DNA Mismatch Repair
Lujan, S. A., & Kunkel, T. A. (2021) · Cells · doi:10.3390/cells10051224 · Cited by 14
Accurate inference of population history in the presence of background selectionPreprint
Cousins, T., Tabin, D. R., Patterson, N. J., Reich, D., & Durvasula, A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.18.576291 · Cited by 14
“We downloaded aligned reads (BAM files) from EBI [55], including 4 chimpanzees (2 female), 6 gorillas (4 female), and 3 orangutans (1 female).”
MethodBrand, C. M., White, F. J., Rogers, A. R., & Webster, T. H. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2200858119 · Cited by 10
Inferring Historical Introgression with Deep Learning
Zhang, Y., Zhu, Q., Shao, Y., Jiang, Y., Ouyang, Y., Zhang, L., & Zhang, W. (2023) · Systematic Biology · doi:10.1093/sysbio/syad033 · Cited by 14
Understanding the Phylogenetics of Indian Hoolock Gibbons: Hoolock hoolock and H. leuconedys
Trivedi, M., Manu, S., Balakrishnan, S., Biswas, J., Asharaf, N. V. K., & Umapathy, G. (2021) · International Journal of Primatology · doi:10.1007/s10764-021-00212-8 · Cited by 13
“9 mya, based on a mutation rate analysis of great apes (Besenbacher et al. 2019).”
BackgroundMethodInfluentialHeadmen, shamans, and mothers: Natural and sexual selection for computational services
Hagen, E. H., Garfield, Z. H., & Lightner, A. D. (2025) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2024.106651 · Cited by 15
Earliest evidence of hominin bipedalism in Sahelanthropus tchadensis
Williams, S. A., Wang, X., Araiza, I., Guerra, J. S., Meyer, M. R., & Spear, J. K. (2026) · Science Advances · doi:10.1126/sciadv.adv0130 · Cited by 12
“The divergence of the hom-inin and panin lineages is known to have occurred late in the Miocene Epoch, roughly 6 to 8 million years ago (Ma) ( 7 , 8 ).”
Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes
Bergman, J., & Schierup, M. H. (2022) · Genome biology · doi:10.1186/s13059-022-02784-x · Cited by 12
Self-citationÁlvarez-Estapé, M., Pawar, H., Fontsere, C., Trujillo, A. E., Gunson, J. L., Bergl, R. A., Bermejo, M., Linder, J. M., McFarland, K., Oates, J. F., et al. (2023) · Genes · doi:10.3390/genes14030743 · Cited by 12
“235 × 10−8 and a 19-year generation time, as previously inferred for gorillas by [50].”
BackgroundWooldridge, T. B., Ford, S. M., Conwell, H. C., Hyde, J. R., Harris, K., & Shapiro, B. (2025) · Molecular Biology and Evolution · doi:10.1093/molbev/msae266 · Cited by 14
Biases in ARG-Based Inference of Historical Population Size in Populations Experiencing Selection
Marsh, J. I., & Johri, P. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae118 · Cited by 11
“…human and other great apes with similar selection (McManus et al. 2015; Cagan et al. 2016; Castellano et al. 2019) and population-genetic dynamics (Besenbacher et al. 2019; Schmidt et al. 2019), we found the greatest driver of population history misinference using Relate was not selection but…”
BackgroundGermline mutation rates and fine-scale recombination parameters in zebra finch
Prentout, D., Bykova, D., Hoge, C., Hooper, D. M., McDiarmid, C. S., Wu, F. L., Griffith, S. C., de Manuel, M., & Przeworski, M. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011661 · Cited by 14
“Given that the sex chromosomes have a lower depth of coverage in the heterogametic sex, making it harder to reliably detect DNMs and recombination events, we focused our analyses on autosomal sequences, as had been done in previous studies (e.g., [30,32,55,113]).”
Yaxley, K. J., & Foley, R. (2019) · Biological Journal of the Linnean Society · doi:10.1093/biolinnean/blz140 · Cited by 11
Amster, G., Murphy, D. A., Milligan, W. R., & Sella, G. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915664117 · Cited by 13
HuConTest: Testing Human Contamination in Great Ape Samples
Kuhlwilm, M., Fontsere, C., Han, S., Álvarez-Estapé, M., & Marquès‐Bonet, T. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab117 · Cited by 9
“A) Schematic tree of the great ape species, with approximate divergence times (Besenbacher et al. 2019).”
BackgroundMethodInfluentialRevisiting the out of Africa event with a deep-learning approach
Montinaro, F., Pankratov, V., Yelmen, B., Pagani, L., & Mondal, M. (2021) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2021.09.006 · Cited by 12
Evidence of Site-Specific and Male-Biased Germline Mutation Rate in a Wild Songbird
Zhang, H., Lundberg, M., Tarka, M., Hasselquist, D., & Hansson, B. (2023) · Genome Biology and Evolution · doi:10.1093/gbe/evad180 · Cited by 12
Novel Integrative Modeling of Molecules and Morphology across Evolutionary TimescalesPreprint
Ogilvie, H., Mendes, F. K., Vaughan, T. G., Matzke, N. J., Stadler, T., Welch, D., & Drummond, A. J. (2018) · ResearchSpace (University of Auckland) · doi:10.1101/242875 · Cited by 10
Franck, M., de Toro‐Martín, J., & Vohl, M. (2022) · Evolutionary Biology · doi:10.1007/s11692-022-09569-x · Cited by 9
Matsudaira, K., & Ishida, T. (2021) · Heredity · doi:10.1038/s41437-021-00452-7 · Cited by 10
Brand, C. M., White, F. J., Ting, N., & Webster, T. H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.14.422788 · Cited by 9
“Homo and Pan diverged ~ 5 to 7 Ma (Sarich and Wilson 1967; Bradley 2008; Scally et al. 2012; Besenbacher et al. 2019) and the most recent estimates for the divergence of bonobos and chimpanzees range between 1 and 2 Ma (Prüfer et al. 2012; de Manuel et al. 2016).”
BackgroundRashid, I., Campos, M., Collier, T. C., Crepeau, M., Weakley, A. M., Gripkey, H., Lee, Y., Schmidt, H., & Lanzaro, G. C. (2022) · Scientific Reports · doi:10.1038/s41598-021-03943-z · Cited by 8
Validation of machine learning approach for direct mutation rate estimation
Burda, K., & Konczal, M. (2023) · Molecular Ecology Resources · doi:10.1111/1755-0998.13841 · Cited by 8
“The mutation rate estimated for the guppy here (2.9 × 10 −9 ) is considerably lower than rates estimated from many other vertebrates, especially primates (humans: 1.22 × 10 −8 from Kessler et al., 2020 , chimpanzee: 1.26 × 10 −8 from Besenbacher et al., 2019).”
InfluentialCampbell, C. R., Tiley, G. P., Poelstra, J. W., Hunnicutt, K. E., Larsen, P. A., Lee, H., Thorne, J. L., dos Reis, M., & Yoder, A. D. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/724880 · Cited by 8
“…a recent investigation of great ape divergence times revealed that lineage-specific mutation rate estimates for chimp, gorilla, and orangutan led to more recent estimates of common ancestor ages compared to those that assumed that all species share the human mutation rate (Besenbacher et al, 2019).”
BackgroundResultInfluentialTRAILS: Tree reconstruction of ancestry using incomplete lineage sorting
Rivas-González, I., Schierup, M. H., Wakeley, J., & Hobolth, A. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1010836 · Cited by 7
“…is well supported by previous studies [53], and is likely because of different branches accumulating a different number of mutations per year, either due to an acceleration or deceleration of the mutational process, changes in the average time of reproduction, or a combination of these [54–56].”
Self-citationParameterizing Pantherinae: De Novo Mutation Rate Estimates from Panthera and Neofelis Pedigrees
Armstrong, E. E., Carey, S. B., Harkess, A., Lazzari, G. Z., Solari, K. A., Maldonado, J. E., Fleischer, R. C., Aziz, N., Walsh, P., Koepfli, K., et al. (2025) · Genome Biology and Evolution · doi:10.1093/gbe/evaf060 · Cited by 8
Population dynamics of GC-changing mutations in humans and great apes
Bergman, J., & Schierup, M. H. (2021) · Genetics · doi:10.1093/genetics/iyab083 · Cited by 8
Self-citationHeredia‐Genestar, J. M., Marquès‐Bonet, T., Juan, D., & Navarro, A. (2020) · Nature Communications · doi:10.1038/s41467-020-16296-4 · Cited by 7
Toward Periodization of the Biosocial Era of the Big History:
Korotayev, A. (2025) · Journal of Big History · doi:10.22339/jbh.v8i2.8201 · Cited by 12
Lee, Y.-L., Bouwman, A. C., Harland, C., Bosse, M., Moreira, G. C. M., Veerkamp, R. F., Mullaart, E., Cambisano, N., Groenen, M. A. M., Karim, L., et al. (2023) · Genome Research · doi:10.1101/gr.277884.123 · Cited by 7
“These revealed large differences in mutation rate across species (e.g., 1.66×10 − 8 in orangutans [Besenbacher et al. 2019] and 0.2×10 − 8 in herrings [Feng et al. 2017]), which may be owing to differences in effective population size and, hence, the effectiveness of purifying selection against…”
InfluentialA curated dataset of great ape genome diversity
Han, S., Riyahi, S., Huang, X., & Kuhlwilm, M. (2025) · Scientific Data · doi:10.1038/s41597-025-06124-z · Cited by 7
“This affects the orangutan individual PD_0262/ORAN23 28,29 , as well as the gorilla individuals Banjo 18,26 , Mimi 18,26 , Mawenzi/PD_0264 26,29 and PD_0189/PD_026 29 , each of which have two unique SRA biosample IDs.”
Unprecedented female mutation bias in the aye-aye, a highly unusual lemur from Madagascar
Wang, R. J., Peña-García, Y., Raveendran, M., Harris, R. A., Nguyen, T. H. D., Gingras, M., Wu, Y., Perez, L. M., Yoder, A. D., Simmons, J. H., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003015 · Cited by 6
“As in previous work, we applied existing strategies that consider differences in coverage and filtering among sites [5,10,11], and that estimate false negative rates from this filtering.”
Morita, W., Morimoto, N., Kono, R. T., & Suwa, G. (2019) · Journal of Human Evolution · doi:10.1016/j.jhevol.2019.102706 · Cited by 5
The PhyloCode : The logical outcome of millennia of evolution of biological nomenclature?
Laurin, M. (2023) · Zoologica Scripta · doi:10.1111/zsc.12625 · Cited by 5
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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