Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales

TLDR

The timing of metazoan divergences is key to animal evolution, yet prior molecular clock studies have been limited by data and methodological biases, producing inconsistent estimates that ignore large fossil uncertainties. The study aims to obtain Bayesian estimates of metazoan divergence times using an unprecedented amount of molecular data and four fossil calibration strategies. The authors combine extensive molecular data with four fossil calibration strategies reflecting disparate interpretations of the metazoan fossil record to perform Bayesian divergence time estimation. The analysis shows that uncertainties in ancient fossils and violations of the molecular clock limit the precision of ancient molecular timescales, making it impossible to pinpoint divergence events accurately enough to test correlations with geological events, and indicating that early animal evolutionary narratives based on molecular clocks are premature.

Abstract

The timing of divergences among metazoan lineages is integral to understanding the processes of animal evolution, placing the biological events of species divergences into the correct geological timeframe. Recent fossil discoveries and molecular clock dating studies have suggested a divergence of bilaterian phyla >100 million years before the Cambrian, when the first definite crown-bilaterian fossils occur. Most previous molecular clock dating studies, however, have suffered from limited data and biases in methodologies, and virtually all have failed to acknowledge the large uncertainties associated with the fossil record of early animals, leading to inconsistent estimates among studies. Here we use an unprecedented amount of molecular data, combined with four fossil calibration strategies (reflecting disparate and controversial interpretations of the metazoan fossil record) to obtain Bayesian estimates of metazoan divergence times. Our results indicate that the uncertain nature of ancient fossils and violations of the molecular clock impose a limit on the precision that can be achieved in estimates of ancient molecular timescales. For example, although we can assert that crown Metazoa originated during the Cryogenian (with most crown-bilaterian phyla diversifying during the Ediacaran), it is not possible with current data to pinpoint the divergence events with sufficient accuracy to test for correlations between geological and biological events in the history of animals. Although a Cryogenian origin of crown Metazoa agrees with current geological interpretations, the divergence dates of the bilaterians remain controversial. Thus, attempts to build evolutionary narratives of early animal evolution based on molecular clock timescales appear to be premature.