Robust Time Estimation Reconciles Views of the Antiquity of Placental Mammals

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.

Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny

“…We estimated the origin of placentals at 88-90 Ma, substantially younger than some previous estimates [5,[14][15][16], but congruent with others [17][18][19].…”

Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas

“…The implied rate decrease (fast in stem monotremes, slow in crown monotremes) for both the nuclear and mitochondrial sequences is 2-to 3-fold greater than decreases across any other node in the tree. A recent study of substitution rates among placental mammals reveals that dramatic rate decreases are far less likely than dramatic rate increases (53), perhaps because the mechanisms involved in DNA copying and repair are far easier to break than to fix.…”

New remains of Eocene and Oligocene Afrosoricida (Afrotheria) from Egypt, with implications for the origin(s) of afrosoricid zalambdodonty

“…The possibility of such a late origin for crown Afro− soricida is strongly contradicted, however, by molecular di− vergence estimates that place the chrysochloroid−tenrecoid split about 40 million years earlier-in either the latest Creta− ceous or earliest Paleocene Gilbert et al 2006;Poux et al 2008). Indeed, the relationship between tenrecs and golden moles is distant enough that the two have not consistently been recovered as sister taxa in molecular phylogenetic analyses (Murata et al 2003;Waddell and Shelley 2003;Kitazoe et al 2007;Arnason et al 2008). It is unlikely that the timing of the chrysochloroid−tenrecoid di− vergence has been dramatically overestimated by these mo− lecular analyses, because dating of other splits within Afro− theria, particularly those within Paenungulata, are generally remarkably consistent with that group's much better fossil record.…”