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.

Figure 1.

The timetree of Primates. Nodes are drawn at their posterior mean ages in millions of years ago (Ma) estimated under the autocorrelated-rates (AR) clock model and calibration strategy A. Filled dots indicate nodes calibrated with the posterior times from the 10-species tree (inset figure), and empty dots indicate nodes with fossil constraints in the 372-species tree. Horizontal bars and numbers in parenthesis represent the 95% posterior CI for the node ages. Numbers associated with branches are ML bootstrap support values of major clades.

Figure 2.

Strepsirrhine portion of the primate timetree (AR clock and calibration strategy A). Legend as for Figure 1.

Figure 3.

Catarrhine portion of the primate timetree (AR clock and calibration strategy A). Legend as for Figure 1.

Figure 4.

Tarsiidae and platyrrhine portion of the primate timetree (AR clock and calibration strategy A). Legend as for Figure 1.

Figure 5.

Effect of calibration strategy and relaxed-clock model. A) Posterior time estimates under fossil calibration strategy A versus time estimates under strategy B, for the AR clock model. B) Posterior time estimates under the AR versus IR clock models, for calibration strategy A.

Figure 6.

Infinite-sites plot. Posterior CI width is plotted against mean posterior divergence times for A) analysis under calibration strategy A and AR clock, and B) analysis under calibration strategy B and AR clock. In both cases, black dots indicate the eight primate nodes shared between the 10-species and 372-species trees, while the grey dots represent the rest of the nodes. Solid line: regression through the origin fitted to the black dots. Dashed line: regression through the origin fitted to all the dots.