Ancient dates or accelerated rates? Morphological clocks and the antiquity of placental mammals

Abstract

Analyses of a comprehensive morphological character matrix of mammals using 'relaxed' clock models (which simultaneously estimate topology, divergence dates and evolutionary rates), either alone or in combination with an 8.5 kb nuclear sequence dataset, retrieve implausibly ancient, Late JurassicEarly Cretaceous estimates for the initial diversification of Placentalia (crown-group Eutheria). These dates are much older than all recent molecular and palaeontological estimates. They are recovered using two very different clock models, and regardless of whether the tree topology is freely estimated or constrained using scaffolds to match the current consensus placental phylogeny. This raises the possibility that divergence dates have been overestimated in previous analyses that have applied such clock models to morphological and total evidence datasets. Enforcing additional age constraints on selected internal divergences results in only a slight reduction of the age of Placentalia. Constraining Placentalia to less than 93.8 Ma, congruent with recent molecular estimates, does not require major changes in morphological or molecular evolutionary rates. Even constraining Placentalia to less than 66 Ma to match the 'explosive' palaeontological model results in only a 10-to 20-fold increase in maximum evolutionary rate for morphology, and fivefold for molecules. The large discrepancies between clock-and fossil-based estimates for divergence dates might therefore be attributable to relatively small changes in evolutionary rates through time, although other explanations (such as overly simplistic models of morphological evolution) need to be investigated. Conversely, dates inferred using relaxed clock models (especially with discrete morphological data and MRBAYES) should be treated cautiously, as relatively minor deviations in rate patterns can generate large effects on estimated divergence dates.

Going underground: postcranial morphology of the early Miocene marsupial mole Naraboryctes philcreaseri and the evolution of fossoriality in notoryctemorphians

“…The mean corresponds to the Triassic-Jurassic boundary, and is broadly congruent with recent molecular estimates for the age of Mammalia (Meredith et al, 2011;dos Reis et al, 2012;. Analysis of eutherian mammals suggests that total evidence dating in which only the age of the root is constrained can result in implausibly ancient divergence dates for at least some nodes (Beck and Lee, 2014); we therefore specified 13 additional topological and temporal constraints on internal nodes, with ages specified as offset exponential priors, namely: Theria, Marsupialia, Didelphidae, Didelphinae, crown-group Australidelphia, Dasyuridae, Dasyurinae, Peramelidae, Diprotodontia, Phalangerida, Petauroidea, Macropodidae and Vombatiformes (see supplementary information for full details). To assist convergence of the Bayesian analyses, monophyly of Eutheria and Metatheria was also enforced a priori, but the ages of these nodes were not calibrated.…”

“…We employed a Bayesian total evidence dating approach (Ronquist et al, 2012a;Beck and Lee, 2014), which simultaneously estimates phylogeny and divergence times for both extant and fossil taxa, as implemented in MrBayes 3.2.2 (Ronquist et al, 2012b). Each terminal taxon was assigned an age: Recent taxa were assigned a point estimate of 0 Ma, whilst each fossil taxon was assigned an age range as a hardbounded uniform prior, based on current age estimates (see supplementary information for full justification).…”

Multiple morphological clocks and total-evidence tip-dating in mammals

“…the common ancestor of placentals is dated at approximately 123 Ma rather than approximately 170 Ma. However, both these total-evidence dates for placental divergences are likely to be overestimates to some extent [9,11]; analyses of huge genomic datasets with robust node calibrations have retrieved ages of approximately 90 Ma [9]. Thus, use of an (arguably) more appropriate multi-clock model [8] exaggerates rather than ameliorates the anomalously deep divergence dates generated by total-evidence analyses.…”

“…The Mk model was used for the morphological data, sampled-ancestor birth -death tree prior was employed, and two nodes (root, stem-therians: figure 2) were calibrated and enforced as monophyletic [11], all other ages and relationships were free to vary. PARTITIONFINDER [12] was used to identify the substitution models for different subsets of the molecular data, using every codon for every locus as a candidate partition and the BIC with unlinked branch lengths, which is most conservative in estimating the number of required partitions.…”

Deciduous dentition and dental eruption of Hyainailouroidea (Hyaenodonta, “Creodonta,” Placentalia, Mammalia)

“…Nonetheless, including deciduous dentition makes it possible to include taxa known primarily from deciduous materials (e.g., Lesmesodon or Pakakali). With the recovery and description of additional deciduous and adult specimens, resolution and support can be expected to improve along with the application of different phylogenetic methods, such as Bayesian "tip-dating" analysis (Beck and Lee, 2014).…”