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A species-level timeline of mammal evolution integrating phylogenomic data

Abstract

High-throughput sequencing projects generate genome-scale sequence data for species-level phylogenies1,2,3. However, state-of-the-art Bayesian methods for inferring timetrees are computationally limited to small datasets and cannot exploit the growing number of available genomes4. In the case of mammals, molecular-clock analyses of limited datasets have produced conflicting estimates of clade ages with large uncertainties5,6, and thus the timescale of placental mammal evolution remains contentious7,8,9,10. Here we develop a Bayesian molecular-clock dating approach to estimate a timetree of 4,705 mammal species integrating information from 72 mammal genomes. We show that increasingly larger phylogenomic datasets produce diversification time estimates with progressively smaller uncertainties, facilitating precise tests of macroevolutionary hypotheses. For example, we confidently reject an explosive model of placental mammal origination in the Palaeogene8 and show that crown Placentalia originated in the Late Cretaceous with unambiguous ordinal diversification in the Palaeocene/Eocene. Our Bayesian methodology facilitates analysis of complete genomes and thousands of species within an integrated framework, making it possible to address hitherto intractable research questions on species diversifications. This approach can be used to address other contentious cases of animal and plant diversifications that require analysis of species-level phylogenomic datasets.

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Fig. 1: Summary of the Bayesian sequential subtree dating approach.
Fig. 2: Bayesian estimation of mammal divergence times.
Fig. 3: Timetree of 4,705 mammal species.

Data availability

All data required to reproduce the analyses are available at https://doi.org/10.6084/m9.figshare.14885691.

Code availability

A repository containing instructions to reproduce the analyses is available at http://github.com/sabifo4/mammals_dating and https://doi.org/10.5281/zenodo.5736629. The MCMCtree software and mcmc3r R package are freely available from http://abacus.gene.ucl.ac.uk/software/paml.html and https://github.com/dosreislab, respectively.

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Acknowledgements

We thank J. Gilbert and C. G. Faulkes for help with the Rodentia subtrees. This work used computing resources from Queen Mary’s Apocrita HPC and University College London Myriad HPC facilities. This work was supported by Biotechnology and Biological Sciences Research Council, UK, awards BB/T01282X/1, BB/T012951/1 and BB/T012773/1.

Author information

Authors and Affiliations

Authors

Contributions

M.d.R. conceived the work. M.d.R., Z.Y., P.C.J.D., S.Á.-C. and A.U.T. designed the analysis. S.Á.-C., A.U.T., R.J.A., P.C.J.D., M.B., E.C. and F.F.N. compiled, processed and verified the molecular and fossil data. S.Á.-C., A.U.T. and M.d.R. analysed the data. M.d.R. and P.C.J.D. wrote the paper with input from all authors.

Corresponding authors

Correspondence to Philip C. J. Donoghue or Mario dos Reis.

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The authors declare no competing interests.

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Nature thanks Olaf Bininda-Emonds, Xing-Xing Shen and the other, anonymous reviewers for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Comparison of prior and posterior times.

a, Prior distribution of node ages generated by MCMC sampling without the molecular alignment. b, Posterior distribution of node ages when the 72-genome alignment is included during MCMC sampling. In both a and b, nodes are plotted at their posterior mean ages. The blue horizontal bars indicate the 95% credibility intervals of node ages.

Extended Data Fig. 2 Impact of fossil calibration strategies on node age estimates.

The posterior of node ages for the 72-taxon phylogeny is estimated using two additional fossil calibration strategies (y-axis) and plotted against the main estimates using best practice in calibration choice39 (x-axis). In all cases the fossil minima are the same, but the calibration maxima changes. In the first strategy (black dots), calibration densities are narrow and close to the fossil ages. A truncated-Cauchy with a short tail (using p = 0 and c = 0.001, which extends the tail to about 110% of the fossil age) is used21. This strategy assumes the fossil record is a good indicator of the true node ages. In the second strategy (red dots), a truncated-Cauchy with a heavy tail (using p = 0.1 and c = 1, which extends the tail to over 900% of the fossil age) is used21. This strategy ignores the presence and absence of stem and sister groups, their palaeoecology, palaeobiogeography, and comparative taphonomy39; and instead, assumes the node ages can be arbitrarily old. Dots are plotted at the posterior mean ages and vertical and horizontal bars indicate 95% CIs. The solid line is the x = y line. The dashed lines are the regression lines for the corresponding data points.

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Supplementary Information

This file contains Supplementary Information, including Supplementary Figs. 1–11, Tables 1–13, annex and additional references.

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Álvarez-Carretero, S., Tamuri, A.U., Battini, M. et al. A species-level timeline of mammal evolution integrating phylogenomic data. Nature 602, 263–267 (2022). https://doi.org/10.1038/s41586-021-04341-1

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