Abstract
BackgroundMolecular studies have reported divergence times of modern placental orders long before the Cretaceous–Tertiary boundary and far older than paleontological data. However, this discrepancy may not be real, but rather appear because of the violation of implicit assumptions in the estimation procedures, such as non-gradual change of evolutionary rate and failure to correct for convergent evolution.Methodology/Principal FindingsNew procedures for divergence-time estimation robust to abrupt changes in the rate of molecular evolution are described. We used a variant of the multidimensional vector space (MVS) procedure to take account of possible convergent evolution. Numerical simulations of abrupt rate change and convergent evolution showed good performance of the new procedures in contrast to current methods. Application to complete mitochondrial genomes identified marked rate accelerations and decelerations, which are not obtained with current methods. The root of placental mammals is estimated to be ∼18 million years more recent than when assuming a log Brownian motion model. Correcting the pairwise distances for convergent evolution using MVS lowers the age of the root about another 20 million years compared to using standard maximum likelihood tree branch lengths. These two procedures combined revise the root time of placental mammals from around 122 million years ago to close to 84 million years ago. As a result, the estimated distribution of molecular divergence times is broadly consistent with quantitative analysis of the North American fossil record and traditional morphological views.Conclusions/SignificanceBy including the dual effects of abrupt rate change and directly accounting for convergent evolution at the molecular level, these estimates provide congruence between the molecular results, paleontological analyses and morphological expectations. The programs developed here are provided along with sample data that reproduce the results of this study and are especially applicable studies using genome-scale sequence lengths.
Highlights
Despite great progress over the past decade, the evolutionary history of placental mammals remains controversial
To improve the detection of, and robustness to, abrupt rate changes, we have developed a new procedure that minimizes the local variability of the inverse of the evolutionary rate
Large nuclear protein datasets of mammals with diverse taxon sampling [e.g., 3, 4] show a large proportion of missing data. Such missing heterogeneous data may lead to complex systematic errors in distance estimation [34]. This is relevant since multidimensional vector space (MVS) analyses work best with low stochastic noise, diverse taxon sampling with a considerable proportion of taxa showing minimal convergent evolution, and minimal bias of the input distances from sources such as missing data
Summary
Despite great progress over the past decade, the evolutionary history of placental mammals remains controversial. Molecular studies have reported divergence times of modern placental orders long before the Cretaceous– Tertiary boundary and far older than paleontological data This discrepancy may not be real, but rather appear because of the violation of implicit assumptions in the estimation procedures, such as non-gradual change of evolutionary rate and failure to correct for convergent evolution. Correcting the pairwise distances for convergent evolution using MVS lowers the age of the root about another 20 million years compared to using standard maximum likelihood tree branch lengths These two procedures combined revise the root time of placental mammals from around 122 million years ago to close to 84 million years ago. The programs developed here are provided along with sample data that reproduce the results of this study and are especially applicable studies using genome-scale sequence lengths
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