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.
Highlights
A parallel challenge to divergence time analysis can be observed in the development of calibration strategies (Marshall 1990; Yang and Rannala 2006; Benton and Donoghue 2007; Marshall 2008; Dornburg et al 2011)
Under calibration strategy A and the autocorrelated rates (AR) model, we find that crown Primates originated 79.2–70.0 million years ago (Ma), before the K–Pg event at 66 Ma
For strategy A, a regression line through the origin fitted to the eight data points is w = 0.128t, meaning that for every 1 million years (My) of divergence, 0.128 My are added to the credibility interval (CI) width (Fig. 6A)
Summary
A parallel challenge to divergence time analysis can be observed in the development of calibration strategies (Marshall 1990; Yang and Rannala 2006; Benton and Donoghue 2007; Marshall 2008; Dornburg et al 2011). The field at present is focused on developing a better understanding of the effects of relaxed clock model choice, and on the impacts of calibration points, both with regard to abundance and placement in the phylogeny In addressing these challenges, it is an open question as to whether simulation studies or tests of empirical data will be more informative for our understanding of best practices. Despite the fact that it is a relatively small and biologically uniform clade, primates have been inordinately and repeatedly the subject of divergence time analysis, with the first studies appearing at the very outset of molecular clock studies (Sarich and Wilson 1967), up to phylogenomic studies encompassing a large set of primate species (Perelman et al 2011; Springer et al 2012). Age estimates for major primate divergence events have varied broadly among different studies (see Table 1), though one result has been relatively constant throughout: primate origins have been typically shown to predate the Cretaceous–Paleogene (K–Pg) mass-extinction event
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