Placental mammal diversification and the Cretaceous-Tertiary boundary

Abstract

Competing hypotheses for the timing of the placental mammal radiation focus on whether extant placental orders originated and diversified before or after the Cretaceous-Tertiary (KT) boundary. Molecular studies that have addressed this issue suffer from single calibration points, unwarranted assumptions about the molecular clock, andor taxon sampling that lacks representatives of all placental orders. We investigated this problem using the largest available molecular data set for placental mammals, which includes segments of 19 nuclear and three mitochondrial genes for representatives of all extant placental orders. We used the ThorneKishino method, which permits simultaneous constraints from the fossil record and allows rates of molecular evolution to vary on different branches of a phylogenetic tree. Analyses that used different sets of fossil constraints, different priors for the base of Placentalia, and different data partitions all support interordinal divergences in the Cretaceous followed by intraordinal diversification mostly after the KT boundary. Four placental orders show intraordinal diversification that predates the KT boundary, but only by an average of 10 million years. In contrast to some molecular studies that date the rat-mouse split as old as 46 million years, our results show improved agreement with the fossil record and place this split at 16-23 million years. To test the hypothesis that molecular estimates of Cretaceous divergence times are an artifact of increased body size subsequent to the KT boundary, we also performed analyses with a "KT body size" taxon set. In these analyses, interordinal splits remained in the Cretaceous.

Figure 1

Simplified versions of three models (1) for the timing and diversification of placental mammals. Red branches indicate intraordinal diversification; green branches indicate interordinal divergences. A simplified time scale is shown below each tree, with an arrow marking the K/T boundary.

Figure 2

Molecular time scale for the orders of placental mammals based on the 16,397-bp data set and maximum likelihood tree of ref. with an opossum outgroup (data not shown), 13 fossil constraints (Materials and Methods), and a mean prior of 105 mya for the placental root. Ordinal designations are listed above the branches. Orange and green lines denote orders with basal diversification before or after the K/T boundary, respectively. Black lines depict orders for which only one taxon was available. Asterisks denote placental taxa included in the “K/T body size” taxon set. The composition of chimeric taxa, including caniform, caviomorph, strepsirrhine, and sirenian, is indicated elsewhere (14). Numbers for internal nodes are cross-referenced in the supporting information.