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.

Tropical heterothermy is “cool”: The expression of daily torpor and hibernation in primates

“…In Madagascar, the geographic home to lemurs, two nonvolant mammalian families have heterothermic members: the Cheirogaleidae (order Primates) and Tenrecidae (order Afrotheria) . Both mammalian groups are hypothesized to have dispersed from continental Africa to Madagascar through independent rafting episodes around 60–50 mya and 40–30 mya, respectively . Tenrecs and cheirogaleids are small‐bodied, nocturnal, and show great flexibility in their heterothermic profiles.…”

“…Tenrecs and cheirogaleids are small‐bodied, nocturnal, and show great flexibility in their heterothermic profiles. Despite those similarities, however, these groups are phylogenetically very distant: whereas tenrecs are an independent lineage within the clade Afrotheria, and may have retained basal placental mammalian traits, cheirogaleids belong to a primate lineage that diverged from other taxa much more recently in evolutionary time . Differences in the physiological tuning of hibernation and metabolic regulation may, in fact, signal variation in underlying mechanisms brought about by unique evolutionary histories, though it is increasingly thought that the capacity for heterothermy is ancestral in mammals, having been suppressed in lineages and species that are apparently nonheterothermic …”

“…The genus Phaner , traditionally included in this family, has been recently linked to another group of nocturnal lemurs, the Lepilemurs . This re‐assignation remains controversial however, and we prefer the traditional taxonomy until such time that this phylogenetic relationship can be more thoroughly studied . The phylogenetic placement of Phaner is relevant for understanding the expression of heterothermy in lemurs because all cheirogaleids, with the exception of Phaner , are believed to be heterothermic to some degree, though little is known of Mirza , the giant mouse lemur, and Allocebus , the hairy‐eared mouse lemur.…”

“…Yet, whether the use of daily torpor or hibernation is considered an ancestral or derived trait within the primates is a subject of debate . Similarities between tenrecs and cheirogaleids could be explained by retention of plesiomorphic traits in both groups, but also it could be explained by convergent evolution, as both small‐bodied heterothermic groups were subjected to similar environmental conditions when they diversified in Madagascar, around the same time during the Miocene . Two contrasting hypotheses are proposed to explain the expression of heterothermy in primates.…”

“…17,18 Both mammalian groups are hypothesized to have dispersed from continental Africa to Madagascar through independent rafting episodes around mya and 40-30 mya, respectively. 19,20 Tenrecs and cheirogaleids are small-bodied, nocturnal, and show great flexibility in their heterothermic profiles. Despite those similarities, however, these groups are phylogenetically very distant: whereas tenrecs are an independent lineage within the clade Afrotheria, and may have retained basal placental mammalian traits, cheirogaleids belong to a primate lineage that diverged from other taxa much more recently in evolutionary time.…”