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      Eutherians experienced elevated evolutionary rates in the immediate aftermath of the Cretaceous–Palaeogene mass extinction

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          Abstract

          The effect of the Cretaceous–Palaeogene (K–Pg) mass extinction on the evolution of many groups, including placental mammals, has been hotly debated. The fossil record suggests a sudden adaptive radiation of placentals immediately after the event, but several recent quantitative analyses have reconstructed no significant increase in either clade origination rates or rates of character evolution in the Palaeocene. Here we use stochastic methods to date a recent phylogenetic analysis of Cretaceous and Palaeocene mammals and show that Placentalia likely originated in the Late Cretaceous, but that most intraordinal diversification occurred during the earliest Palaeocene. This analysis reconstructs fewer than 10 placental mammal lineages crossing the K–Pg boundary. Moreover, we show that rates of morphological evolution in the 5 Myr interval immediately after the K–Pg mass extinction are three times higher than background rates during the Cretaceous. These results suggest that the K–Pg mass extinction had a marked impact on placental mammal diversification, supporting the view that an evolutionary radiation occurred as placental lineages invaded new ecological niches during the Early Palaeocene.

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          The delayed rise of present-day mammals.

          Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.
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            The placental mammal ancestor and the post-K-Pg radiation of placentals.

            To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.
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              Effects of size and temperature on developmental time.

              Body size and temperature are the two most important variables affecting nearly all biological rates and times. The relationship of size and temperature to development is of particular interest, because during ontogeny size changes and temperature often varies. Here we derive a general model, based on first principles of allometry and biochemical kinetics, that predicts the time of ontogenetic development as a function of body mass and temperature. The model fits embryonic development times spanning a wide range of egg sizes and incubation temperatures for birds and aquatic ectotherms (fish, amphibians, aquatic insects and zooplankton). The model also describes nearly 75% of the variation in post-embryonic development among a diverse sample of zooplankton. The remaining variation is partially explained by stoichiometry, specifically the whole-body carbon to phosphorus ratio. Development in other animals at other life stages is also described by this model. These results suggest a general definition of biological time that is approximately invariant and common to all organisms.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                29 June 2016
                29 June 2016
                : 283
                : 1833
                : 20153026
                Affiliations
                [1 ]Department of Earth Sciences, University College London , Gower Street, London WC1E 6BT, UK
                [2 ]Department of Genetics, Evolution and Environment, University College London , Gower Street, London WC1E 6BT, UK
                Author notes
                Author information
                http://orcid.org/0000-0002-4077-732X
                Article
                rspb20153026
                10.1098/rspb.2015.3026
                4936024
                27358361
                1ce3918d-28ac-48e7-a8be-3de746cde3c3
                © 2016 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 17 December 2015
                : 26 May 2016
                Funding
                Funded by: Natural Environment Research Council, http://dx.doi.org/10.13039/501100000270;
                Award ID: NE/J500136/1
                Categories
                1001
                70
                144
                Research Articles
                Custom metadata
                June 29, 2016

                Life sciences
                mammals,evolutionary rate,extinction,radiation,cretaceous,palaeogene
                Life sciences
                mammals, evolutionary rate, extinction, radiation, cretaceous, palaeogene

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