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

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          Summary

          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.

          Highlights

          • Molecular clock analysis indicates an ancient origin of animals in the Cryogenian

          • Diversification into animal phyla occurred in the Ediacaran, before the Cambrian

          • Uncertainties in the fossil record and the molecular clock affect time estimates

          • A precise timeline of animal evolution cannot be obtained with current methods

          Abstract

          dos Reis et al. study the uncertainty in Bayesian estimates of the time of origin of animals using phylogenomic data. They find that disentangling the timeline of early animal evolution is hard given the large uncertainty associated with the fossil record of early animals and the strong violation of the molecular clock in ancient phylogenies.

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          The Cambrian conundrum: early divergence and later ecological success in the early history of animals.

          Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.
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            An algorithm for progressive multiple alignment of sequences with insertions.

            Dynamic programming algorithms guarantee to find the optimal alignment between two sequences. For more than a few sequences, exact algorithms become computationally impractical, and progressive algorithms iterating pairwise alignments are widely used. These heuristic methods have a serious drawback because pairwise algorithms do not differentiate insertions from deletions and end up penalizing single insertion events multiple times. Such an unrealistically high penalty for insertions typically results in overmatching of sequences and an underestimation of the number of insertion events. We describe a modification of the traditional alignment algorithm that can distinguish insertion from deletion and avoid repeated penalization of insertions and illustrate this method with a pair hidden Markov model that uses an evolutionary scoring function. In comparison with a traditional progressive alignment method, our algorithm infers a greater number of insertion events and creates gaps that are phylogenetically consistent but spatially less concentrated. Our results suggest that some insertion/deletion "hot spots" may actually be artifacts of traditional alignment algorithms.
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              A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

              Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                16 November 2015
                16 November 2015
                : 25
                : 22
                : 2939-2950
                Affiliations
                [1 ]Department of Genetics, Evolution, and Environment, University College London, Gower Street, London WC1E 6BT, UK
                [2 ]School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
                [3 ]School of Earth Sciences, University of Bristol, Life Sciences Building, Tyndall Avenue, Bristol BS8 1TQ, UK
                Author notes
                []Corresponding author phil.donoghue@ 123456bristol.ac.uk
                [∗∗ ]Corresponding author z.yang@ 123456ucl.ac.uk
                Article
                S0960-9822(15)01177-X
                10.1016/j.cub.2015.09.066
                4651906
                26603774
                4192dfaa-8ef5-435e-8d3b-91895e82e499
                © 2015 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 9 June 2015
                : 20 September 2015
                : 22 September 2015
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                Life sciences
                Life sciences

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