Using Phylogenomic Data to Explore the Effects of Relaxed Clocks and Calibration Strategies on Divergence Time Estimation: Primates as a Test Case

Abstract

Primates have long been a test case for the development of phylogenetic methods for divergence time estimation. Despite a large number of studies, however, the timing of origination of crown Primates relative to the Cretaceous-Paleogene (K-Pg) boundary and the timing of diversification of the main crown groups remain controversial. Here, we analysed a data set of 372 taxa (367 Primates and 5 outgroups, 3.4 million aligned base pairs) that includes nine primate genomes. We systematically explore the effect of different interpretations of fossil calibrations and molecular clock models on primate divergence time estimates. We find that even small differences in the construction of fossil calibrations can have a noticeable impact on estimated divergence times, especially for the oldest nodes in the tree. Notably, choice of molecular rate model (autocorrelated or independently distributed rates) has an especially strong effect on estimated times, with the independent rates model producing considerably more ancient age estimates for the deeper nodes in the phylogeny. We implement thermodynamic integration, combined with Gaussian quadrature, in the program MCMCTree, and use it to calculate Bayes factors for clock models. Bayesian model selection indicates that the autocorrelated rates model fits the primate data substantially better, and we conclude that time estimates under this model should be preferred. We show that for eight core nodes in the phylogeny, uncertainty in time estimates is close to the theoretical limit imposed by fossil uncertainties. Thus, these estimates are unlikely to be improved by collecting additional molecular sequence data. All analyses place the origin of Primates close to the K-Pg boundary, either in the Cretaceous or straddling the boundary into the Palaeogene.

References 158

1. 1.

   Alfaro M.E., Santini F., Brock C., Alamillo H., Dornburg A., Rabosky D.L., Carnevale G., Harmon L.J. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.Proc. Natl. Acad. Sci.USA106:13410–13414.

   Not in our library10.1073/pnas.0811087106

2. 2.

   Andersen M.J., Shult H.T., Cibois A., Thibault J.C., Filardi C.E., Moyle R.G. 2015. Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus).R. Soc. Open Sci.,2:140375.

   Not in our library10.1098/rsos.140375

3. 3.

   Aris-Brosou S., Yang Z. 2002. Effects of models of rate evolution on estimation of divergence dates with special reference to the metazoan 18S ribosomal RNA phylogeny.Syst. Biol.51:703–714.

   Not in our library10.1080/10635150290102375

4. 4.

   Badgley C., Behrensmeyer A.K. 1995. Two long geological records of continental ecosystems.Palaeogeogr. Palaeoclimatol. Palaeoecol.115:1–11.

   Not in our library

5. 5.

   Baele G., Lemey P., Bedford T., Rambaut A., Suchard M.A., Alekseyenko A.V. 2012a. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty.Mol. Biol. Evol.29:2157–2167.

   Not in our library10.1093/molbev/mss084

6. 6.

   Baele G., Li W.L.S., Drummond A.J., Suchard M.A., Lemey P. 2012b. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics.Mol. Biol. Evol.30:239–243.

   Not in our library10.1093/molbev/mss243

7. 7.

   Beard K. 1998. A new genus of Tarsiidae (Mammalia: Primates) from the middle Eocene of Shanxi Province, China, with notes on the historical biogeography of tarsiers.Bull. Carnegie Mus. Nat. Hist.34:260–277.

   Not in our library

8. 8.

   Beard K.C. 2016. Out of Asia: Anthropoid origins and the colonization of Africa.Annu. Rev. Anthropol.,45:13.1–13.15.

   Not in our library

9. 9.

   Beard K.C., Qi T., Dawson M.R., Wang B., Li C. 1994. A diverse new primate fauna from middle Eocene fissure-fillings in southeastern China.Nature368:604–609.

   Not in our library10.1038/368604a0

10. 10.

    Begun D.R. 2010. Miocene hominids and the origins of the African apes and humans.Annu. Rev. Anthropol.39:67–84.

    Not in our library

11. 11.

    Begun D.R., Nargolwalla M.C., Kordos L. 2012. European Miocene hominids and the origin of the African ape and human clade.Evol. Anthropol.21:10–23.

    Not in our library10.1002/evan.20329

12. 12.

    Benefit B.R., Pickford M. 1986. Miocene fossil cercopithecoids from Kenya.Am. J. Phys. Anthropol.69:441–464.

    Not in our library

13. 13.

    Benton M.J., Donoghue P.C. 2007. Paleontological evidence to date the tree of life.Mol. Biol. Evol.24:26–53.

    Not in our library10.1093/molbev/msl150

14. 14.

    Benton M.J., Donoghue P.C.J., Asher R.J. 2009. Calibrating and constraining molecular clocks. In: Hedges B.S., Kumar S., editors. The timetree of life.Oxford, England: Oxford University Press. p. 35–86.

    Not in our library

15. 15.

    Bininda-Emonds O.R., Cardillo M., Jones K.E., MacPhee R.D., Beck R.M., Grenyer R., Price S.A., Vos R.A., Gittleman J.L., Purvis A. 2007. The delayed rise of present-day mammals.Nature446:507–512.

    Not in our library10.1038/nature05634

16. 16.

    Bishop W. 1962. The mammalian fauna and geomorphological relations of the Napak volcanics, Karamoja.Geol. Surv. Uganda Rec.1957–1958:1–18.

    Not in our library

17. 17.

    Bloch J.I., Silcox M.T., Boyer D.M., Sargis E.J. 2007. New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates.Proc. Natl. Acad. Sci.USA104:1159–1164.

    Not in our library10.1073/pnas.0610579104

18. 18.

    Bloch J.I., Woodruff E.D., Wood A.R., Rincon A.F., Harrington A.R., Morgan, Gary S. Foster, David A. Camilo Montes, Jaramillo, Carlos A. Jud, Nathan A. Jones Douglas S. & MacFadden Bruce J. 2016. First North American fossil monkey and early Miocene tropical biotic interchange.Nature533:243–246.

    Not in our library10.1038/nature17415

19. 19.

    Bond M., Tejedor M.F., Campbell K.E. Jr., Chornogubsky L., Novo N., Goin F. 2015. Eocene primates of South America and the African origins of New World monkeys.Nature520:538–541.

    Not in our library10.1038/nature14120

20. 20.

    Bown T.M., Fleagle J.G. 1993. Systematics, biostratigraphy, and dental evolution of the Palaeothentidae, later Oligocene to early-middle Miocene (Deseadan-Santacrucian) caenolestoid marsupials of South America.J. Paleontol.2 Suppl:1–76.

    Not in our library

21. 21.

    Brunet M., Guy F., Pilbeam D., Lieberman D.E., Likius A., Mackaye H.T., Ponce de Leon M.S., Zollikofer C.P., Vignaud P. 2005. New material of the earliest hominid from the Upper Miocene of Chad.Nature434:752–755.

    Not in our library10.1038/nature03392

22. 22.

    Brunet M., Guy F., Pilbeam D., Mackaye H.T., Likius A., Ahounta D., Beauvilain A., Blondel C., Bocherens H., Boisserie J.-R., Louis De Bonis, Yves Coppens, Jean Dejax, Christiane Denys, Philippe Duringer, Véra Eisenmann, Gongdibé Fanone, Pierre Fronty, Denis Geraads, Thomas Lehmann, Fabrice Lihoreau, Antoine Louchart, Adoum Mahamat, Gildas Merceron, Guy Mouchelin, Olga Otero, Pablo Pelaez Campomanes, Marcia Ponce De Leon, Jean-Claude Rage, Michel Sapanet, Mathieu Schuster, Jean Sudre, Pascal Tassy, Xavier Valentin, Patrick Vignaud, Laurent Viriot, Antoine Zazzo, Christoph Zollikofer. 2002. A new hominid from the upper Miocene of Chad, Central Africa.Nature418:145–151.

    Not in our library10.1038/nature00879

23. 23.

    Buckley G.A. 1997. A new species of Purgatorius (Mammalia; Primatomorpha) from the lower Paleocene Bear formation, Crazy Mountains basin, south-central Montana.J. Paleontol.71: 149–155.

    Not in our library

24. 24.

    Burgess R., Yang Z. 2008. Estimation of hominoid ancestral population sizes under Bayesian coalescent models incorporating mutation rate variation and sequencing errors.Mol. Biol. Evol.25: 1979–1994.

    Not in our library10.1093/molbev/msn148

25. 25.
    Estimating the phylogeny and divergence times of primates using a supermatrix approach · 2009

    No notice
26. 26.

    Chester S.G., Bloch J.I., Boyer D.M., Clemens W.A. 2015. Oldest known euarchontan tarsals and affinities of Paleocene Purgatorius to Primates.Proc. Natl. Acad. Sci.USA112:1487–1492.

    Not in our library10.1073/pnas.1421707112

27. 27.

    Clemens W.A. 1974. Purgatorius, an early paromomyid primate (Mammalia).Science184:903–905.

    Not in our library10.1126/science.184.4139.903

28. 28.

    Clemens W.A. 2004. Purgatorius (Plesiadapiformes, Primates, Mammalia), a Paleocene immigrant into northeastern Montana: stratigraphic occurrences and incisor proportions.Bull. Carnegie Mus. Nat. His.36:3–13.

    Not in our library

29. 29.

    Corruccini R.S., Baba M., Goodman M., Ciochon R.L., Cronin J.E. 1980. Non-linear macromolecular evolution and the molecular clock.Evolution34:1216–1219.

    Not in our library10.1111/j.1558-5646.1980.tb04069.x

30. 30.

    de Queiroz A. 2005. The resurrection of oceanic dispersal in historical biogeography.Trends Ecol. Evol.20:68–73

    Not in our library10.1016/j.tree.2004.11.006

31. 31.

    de Queiroz A. 2014. The monkey’s voyage: how improbable journeys shaped the history of life.New York: Basic Books.

    Not in our library

32. 32.

    Dornburg A, Beaulieu J.M., Oliver J.C., Near T.J. 2011. Integrating fossil preservation biases in the selection of calibrations for molecular divergence time estimation.Syst. Biol.60:519–527.

    Not in our library10.1093/sysbio/syr019

33. 33.

    dos Reis M., Donoghue P.C., Yang Z. 2014a. Neither phylogenomic nor palaeontological data support a Palaeogene origin of placental mammals.Biol. Lett.10:20131003.

    Not in our library10.1098/rsbl.2013.1003

34. 34.

    dos Reis M., Donoghue P.C., Yang Z. 2016. Bayesian molecular clock dating of species divergences in the genomics era.Nat. Rev. Genet.17:71–80.

    Not in our library10.1038/nrg.2015.8

35. 35.

    dos Reis M., Inoue J., Hasegawa M., Asher R., Donoghue P.C., Yang Z. 2012. Phylogenomic data sets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny.Proc. R. Soc. Lond. B Biol. Sci.279:3491–3500.

    Not in our library10.1098/rspb.2012.0683

36. 36.
    Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales · 2015

    No notice
37. 37.

    dos Reis M., Yang Z. 2011. Approximate likelihood calculation for Bayesian estimation of divergence times.Mol. Biol. Evol.28:2161–2172.

    Not in our library10.1093/molbev/msr045

38. 38.

    dos Reis M., Yang Z. 2013. The unbearable uncertainty of Bayesian divergence time estimation.J. Syst. Evol.51:30–43.

    Not in our library

39. 39.

    dos Reis M., Zhu T., Yang Z. 2014b. The impact of the rate prior on Bayesian estimation of divergence times with multiple loci.Syst. Biol.63:555–565.

    Not in our library10.1093/sysbio/syu020

40. 40.
    Relaxed Phylogenetics and Dating with Confidence · 2006

    No notice

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