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

Abstract

SummaryThe 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.

Biosilicification Drives a Decline of Dissolved Si in the Oceans through Geologic Time

“…Molecular clocks use the mutation rate of biomolecules to deduce the time in prehistory when two or more life forms diverged. The main problems with molecular clocks include differences in fossil-based calibration points, differences in molecular clock rate models, differences in amino acid substitution rates among various parts of the dataset and uncertainty in the phylogenetic tree, thus limiting the precision that can be achieved in estimates of ancient molecular timescales (dos Reis et al, 2015). Cyanobacteria are at least 2.3-3 Ga old from molecular clock studies (Dvorák et al, 2014;Sanchez-Baracaldo, 2015), whereas fossil evidence (stromatolites, microfossils, carbon isotopes, biomarkers, signs of oxygen) from Greenland, Australia and elsewhere have raised the possibility of cyanobacteria older than 3 Gy, although these claims are disputed (Schirrmeister et al, 2016).…”

Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil

“…Molecular clock analyses predict an earlier, pre-Ediacaran origin for the Metazoa and Eumetazoa, and an early Ediacaran origin for Bilateria, Protostomia and Deuterostomia 18 . Palaeontological Nature ecology & evolutioN support for these suggestions is limited to purported body fossils of sponges 19 and demosponge biomarkers 20 .…”

“…A considerable gap therefore remains between the fossil record of the late Ediacaran and molecular clock estimates for deep splits in the animal tree, for example the origin of Metazoa and Eumetazoa 3 . Assuming that contemporary molecular clock analyses yield accurate, if imprecise 18 , node ages for animal divergences, a small body size and concomitant limited fossilization potential 21 could reconcile these discordant records of animal evolution (but see ref. 22 ).…”

Ediacaran developmental biology

“…Molecular clock estimates suggest that animals originated ∼700–800 million years ago (Ma) (dos Reis et al ., 2015), but unequivocal fossil evidence for animals is not found until closer to ∼541 Ma (e.g. Erwin et al ., 2011; Cunningham et al ., 2017).…”