Total-Evidence Dating Under the Fossilized Birth-Death Process

Bayesian total-evidence dating involves the simultaneous analysis of morphological data from the fossil record and morphological and sequence data from recent organisms, and it accommodates the uncertainty in the placement of fossils while dating the phylogenetic tree. Due to the flexibility of the Bayesian approach, total-evidence dating can also incorporate additional sources of information. Here, we take advantage of this and expand the analysis to include information about fossilization and sampling processes. Our work is based on the recently described fossilized birth-death (FBD) process, which has been used to model speciation, extinction, and fossilization rates that can vary over time in a piecewise manner. So far, sampling of extant and fossil taxa has been assumed to be either complete or uniformly at random, an assumption which is only valid for a minority of data sets. We therefore extend the FBD process to accommodate diversified sampling of extant taxa, which is standard practice in studies of higher-level taxa. We verify the implementation using simulations and apply it to the early radiation of Hymenoptera (wasps, ants, and bees). Previous total-evidence dating analyses of this data set were based on a simple uniform tree prior and dated the initial radiation of extant Hymenoptera to the late Carboniferous (309 Ma). The analyses using the FBD prior under diversified sampling, however, date the radiation to the Triassic and Permian (252 Ma), slightly older than the age of the oldest hymenopteran fossils. By exploring a variety of FBD model assumptions, we show that it is mainly the accommodation of diversified sampling that causes the push toward more recent divergence times. Accounting for diversified sampling thus has the potential to close the long-discussed gap between rocks and clocks. We conclude that the explicit modeling of fossilization and sampling processes can improve divergence time estimates, but only if all important model aspects, including sampling biases, are adequately addressed.