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

Mario Dos Reis,Yuttapong Thawornwattana,Konstantinos Angelis,Maximilian J Telford,Philip C.J Donoghue,Ziheng Yang

doi:10.1016/j.cub.2015.09.066

Mario Dos Reis, Yuttapong Thawornwattana + Show 4 more

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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.

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The timing and tempo of the evolutionary emergence of animal biodiversity has been among the most enduring problems in evolutionary biology
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
Most previous molecular clock dating studies, 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

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The timing and tempo of the evolutionary emergence of animal biodiversity has been among the most enduring problems in evolutionary biology. But not necessarily mutually exclusive, triggers for animal diversification include the release of their forebears from the environmental strictures of the Cryogenian or Ediacaran Snowball Earth [5, 6] and the effects of cosmic radiation [7], polar wander [8], continental fragmentation [9], H2S toxicity [10], salinity [11, 12], a scarcity of trace metal micronutrients [13], a pulse of continental weathering yielding nutrients to the oceans [14], global warming [15], or an escalatory predator-prey arms race [16, 17] These hypotheses propose more or less proximal causal mechanistic relationships with metazoan diversification, they rely on presumed temporal coincidence. Reconciling these competing hypotheses requires calibration to a common absolute timescale

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