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      Resolving the relationships of Paleocene placental mammals

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          ABSTRACT

          The ‘Age of Mammals’ began in the Paleocene epoch, the 10 million year interval immediately following the Cretaceous–Palaeogene mass extinction. The apparently rapid shift in mammalian ecomorphs from small, largely insectivorous forms to many small‐to‐large‐bodied, diverse taxa has driven a hypothesis that the end‐Cretaceous heralded an adaptive radiation in placental mammal evolution. However, the affinities of most Paleocene mammals have remained unresolved, despite significant advances in understanding the relationships of the extant orders, hindering efforts to reconstruct robustly the origin and early evolution of placental mammals. Here we present the largest cladistic analysis of Paleocene placentals to date, from a data matrix including 177 taxa (130 of which are Palaeogene) and 680 morphological characters. We improve the resolution of the relationships of several enigmatic Paleocene clades, including families of ‘condylarths’. Protungulatum is resolved as a stem eutherian, meaning that no crown‐placental mammal unambiguously pre‐dates the Cretaceous–Palaeogene boundary. Our results support an Atlantogenata–Boreoeutheria split at the root of crown Placentalia, the presence of phenacodontids as closest relatives of Perissodactyla, the validity of Euungulata, and the placement of Arctocyonidae close to Carnivora. Periptychidae and Pantodonta are resolved as sister taxa, Leptictida and Cimolestidae are found to be stem eutherians, and Hyopsodontidae is highly polyphyletic. The inclusion of Paleocene taxa in a placental phylogeny alters interpretations of relationships and key events in mammalian evolutionary history. Paleocene mammals are an essential source of data for understanding fully the biotic dynamics associated with the end‐Cretaceous mass extinction. The relationships presented here mark a critical first step towards accurate reconstruction of this important interval in the evolution of the modern fauna.

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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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              Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny.

              The fossil record suggests a rapid radiation of placental mammals following the Cretaceous-Paleogene (K-Pg) mass extinction 65 million years ago (Ma); nevertheless, molecular time estimates, while highly variable, are generally much older. Early molecular studies suffer from inadequate dating methods, reliance on the molecular clock, and simplistic and over-confident interpretations of the fossil record. More recent studies have used Bayesian dating methods that circumvent those issues, but the use of limited data has led to large estimation uncertainties, precluding a decisive conclusion on the timing of mammalian diversifications. Here we use a powerful Bayesian method to analyse 36 nuclear genomes and 274 mitochondrial genomes (20.6 million base pairs), combined with robust but flexible fossil calibrations. Our posterior time estimates suggest that marsupials diverged from eutherians 168-178 Ma, and crown Marsupialia diverged 64-84 Ma. Placentalia diverged 88-90 Ma, and present-day placental orders (except Primates and Xenarthra) originated in a ∼20 Myr window (45-65 Ma) after the K-Pg extinction. Therefore we reject a pre K-Pg model of placental ordinal diversification. We suggest other infamous instances of mismatch between molecular and palaeontological divergence time estimates will be resolved with this same approach.
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                Author and article information

                Contributors
                thomas.halliday.11@ucl.ac.uk
                Journal
                Biol Rev Camb Philos Soc
                Biol Rev Camb Philos Soc
                10.1111/(ISSN)1469-185X
                BRV
                Biological Reviews of the Cambridge Philosophical Society
                Blackwell Publishing Ltd (Oxford, UK )
                1464-7931
                1469-185X
                21 December 2015
                February 2017
                : 92
                : 1 ( doiID: 10.1111/brv.2017.92.issue-1 )
                : 521-550
                Affiliations
                [ 1 ] Department of Earth Sciences University College London Gower Street London WC1E 6BT U.K.
                [ 2 ] Department of Genetics, Evolution and Environment University College London Gower Street London WC1E 6BT U.K.
                Author notes
                [*] [* ]Address for correspondence (Tel: +44 20 7679 7117; E‐mail: thomas.halliday.11@ 123456ucl.ac.uk ).
                Author information
                http://orcid.org/0000-0002-4077-732X
                Article
                BRV12242
                10.1111/brv.12242
                6849585
                28075073
                68cb9f91-f481-44ec-9101-8d3949014e19
                © 2015 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 May 2015
                : 28 October 2015
                : 04 November 2015
                Page count
                Figures: 4, Tables: 3, Pages: 30, Words: 25716
                Funding
                Funded by: NERC Award , open-funder-registry 10.13039/501100000270;
                Award ID: NE/J/500136/1
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                February 2017
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:12.11.2019

                Ecology
                placentalia,evolution,phylogeny,palaeogene,radiation,condylarthra,palaeontology
                Ecology
                placentalia, evolution, phylogeny, palaeogene, radiation, condylarthra, palaeontology

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