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Constraints on the Timescale of Animal Evolutionary History

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Constraints on the Timescale of Animal Evolutionary History Palaeontologia Electronica palaeo-electronica.org Constraints on the timescale of animal evolutionary history Michael J. Benton, Philip C.J. Donoghue, Robert J. Asher, Matt Friedman, Thomas J. Near, and Jakob Vinther ABSTRACT Dating the tree of life is a core endeavor in evolutionary biology. Rates of evolution are fundamental to nearly every evolutionary model and process. Rates need dates. There is much debate on the most appropriate and reasonable ways in which to date the tree of life, and recent work has highlighted some confusions and complexities that can be avoided. Whether phylogenetic trees are dated after they have been estab- lished, or as part of the process of tree finding, practitioners need to know which cali- brations to use. We emphasize the importance of identifying crown (not stem) fossils, levels of confidence in their attribution to the crown, current chronostratigraphic preci- sion, the primacy of the host geological formation and asymmetric confidence intervals. Here we present calibrations for 88 key nodes across the phylogeny of animals, rang- ing from the root of Metazoa to the last common ancestor of Homo sapiens. Close attention to detail is constantly required: for example, the classic bird-mammal date (base of crown Amniota) has often been given as 310-315 Ma; the 2014 international time scale indicates a minimum age of 318 Ma. Michael J. Benton. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. [email protected] Philip C.J. Donoghue. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. [email protected] Robert J. Asher, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, U.K. [email protected] Matt Friedman, Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, OX1 3AN, U.K. [email protected] Thomas J. Near, Department of Ecology and Evolutionary Biology, Yale University, P. O. Box 208106, 165 Prospect Street, New Haven, CT 06520-8106, U.S.A. [email protected] Jakob Vinther. School of Earth Sciences, University of Bristol, Bristol, BS8 1RJ, U.K. [email protected] PE Article Number: 18.1.1FC Copyright: Society for Vertebrate Paleontology February 2015 Submission: 1 August 2013. Acceptance: 7 December 2014 Benton, Michael J., Donoghue, Philip C.J., Asher, Robert J., Friedman, Matt, Near, Thomas J., and Vinther, Jakob. 2015. Constraints on the timescale of animal evolutionary history. Palaeontologia Electronica 18.1.1FC; 1-106; palaeo-electronica.org/content/fc-1 Calibrations published in the Fossil Calibration Series are accessioned into the Fossil Calibration Database (www.fossilcalibra- tions.org). The Database is a dynamic tool for finding up-to-date calibrations, and calibration data will be updated and annotated as interpretations change. In contrast, the Fossil Calibration papers are a permanent published record of the information on which the cal- ibrations were originally based. Please refer to the Database for the latest data. BENTON ET AL.: ANIMAL HISTORY TIMESCALE KEYWORDS: phylogeny; calibration; animals; Metazoa; birds; mammals INTRODUCTION The fundamental division of Metazoa (Figure 1) is comprised of sponges, chordates, their last com- This contribution represents one of a series, mon ancestor and all of its descendants. The with calibration dates assessed and presented monophyly of Metazoa is widely accepted, sub- according to the principles enunciated by Parham stantiated on the basis of both molecular and phe- et al. (2012). The paper has evolved from earlier notypic data (Eernisse and Peterson, 2004; efforts (Benton and Donoghue, 2007; Donoghue Halanych, 2004; Philippe et al., 2009; Edgecombe and Benton, 2007; Benton et al., 2009) and has et al., 2011). Metazoa is comprised of Bilateria/ been augmented by the addition of relevant nodes Nephrozoa (chordates, arthropods, their last com- and authors. mon ancestor and all of its descendants) plus Here we present calibrations for 88 key Cnidaria, Placozoa, Ctenophora, and sponges (the nodes, with a strong focus on vertebrates, reflect- monophyly or paraphyly of which remains conten- ing current phylogenomic interest. There are 11 tious). Bilateria is divided into the two major clades node calibrations for basal animal clades, 8 for Protostomia (arthropods, annelids, their last com- deuterostomes and basal chordates, 21 for gnatho- mon ancestor and its descendants) and Deuteros- stomes and fishes, 6 for basal tetrapods, 6 for rep- tomia (Echinodermata, Hemichordata, Aco- tiles/amniotes, 4 for birds, and 32 for mammals. elomorpha, Chordata). Protostomia comprises Some of the calibrations given here have been Ecdysozoa (Arthropoda, Kinorhyncha, Loricifera, included in previous compendia (e.g., Benton and Nematoda, Nematomorpha, Onychophora, Pria- Donoghue, 2007; Benton et al., 2009; Dos Reis et pulida, Tardigrada) and Lophotrochozoa (Annelida, al., 2012; Near et al., 2012), but they are all revised Brachiopoda, Ectoprocta, Entoprocta, Gastrotricha, in terms of key fossils, regional dating of forma- Gnathostomulida, Mollusca, Nemertini, Phoronida, tions, and the new international time scale (Grad- Platyhelminthes, Rotifera, Sipuncula). stein et al., 2012; as updated in the ‘International Chronostratigraphic Chart’, last version consulted, Deuterostomes and Basal Chordates v2014/10). We reverse the order of entries com- Deuterostomia comprises chordates, echino- pared to our previous reports, reflecting now a phy- derms, hemichordates (Figure 2) and probably logenetic sequence from the bottom up, rather than Acoelomorpha. Traditionally, hemichordates were a hominid-focused approach from Homo sapiens paired with chordates to the exclusion of echino- towards ever more distant clades. Nodes are num- derms, but the consensus of morphological and bered in sequence, and keyed to the tree diagrams molecular studies (e.g., Eernisse and Peterson, throughout the paper. 2004; Delsuc et al., 2006; Swalla and Smith, 2008; All calibrations are dependent on phylogeny. Cannon et al., 2009; Edgecombe et al., 2011; Röt- Differing clade boundaries can affect the position of tinger and Lowe, 2012) now pairs hemichordates a fossil, and so its role in fixing dates. We have with echinoderms as the clade Ambulacraria. paid attention to all current phylogenetic hypothe- Chordates have long been understood to ses for all clades considered, and we present what include vertebrates, cephalochordates (amphi- we regard as the best current consensus on the oxus) and tunicates (sea squirts). The relative phylogeny of each group, incorporating both ordering of these had been debated, with Cephalo- molecular and morphological data. Thus key chordata traditionally grouped with Vertebrata to sources for each phylogeny are specified. the exclusion of Tunicata. Molecular work (e.g., We begin with an overview of the phyloge- Eernisse and Peterson, 2004; Delsuc et al., 2006; netic justifications that underpin the major clades, Swalla and Smith, 2008; Cannon et al., 2009; and follow with the calibration of key nodes in the Edgecombe et al., 2011; Röttinger and Lowe, history of animal life. 2012) places cephalochordates as the sister clade to Tunicata plus Vertebrata, as clade Olfactores. PHYLOGENETIC OVERVIEW The relationships of the basal vertebrates to Animals each other have been controversial. For a long time, zoologists grouped the living lampreys and Animals (Metazoa) are generally motile het- hagfishes together as Cyclostomata. The first cla- erotrophs, distinguished from Fungi and plants. 2 PALAEO-ELECTRONICA.ORG Porifera Anthozoa Olivooides multisulcatus (3) 529 Medusozoa Scalidophora Nematoidea Tardigrada Onychophora Ecdysozoa ‘Rusophycus’ PanArthropoda Chelicerata Lobopodia (6, 7) 528.82 Arthropoda Myriapoda Mandibulata PanCrustacea Malacostraca Eumetazoa Metazoa Yicaris dianensis (8) 514 other PanCrustacea Protostomes Gastropoda (10) 532 Aldanella Bivalvia Mollusca Scaphopoda Lophotrochozoa Acuilifera Cephalopoda (1, 2, 4, 5, 9) 552.85 Sedentaria Annelida “Xanioprion” vivei (11) 476.5 Errantia Kimberella quadrata Deuterostomes FIGURE 1. Calibration diagram for metazoans. distic studies considered Cyclostomata paraphy- cyclostome monophyly versus paraphyly). The sta- letic, generally recognizing a closer relationship tistical significance of these apomorphies has been between lampreys and Gnathostomata, than hag- contested by Thompson et al. (2014). These phylo- fishes. Molecular phylogenetic studies generally genetic issues are important as they affect the recover a monophyletic Cyclostomata (reviewed by placement of fossils relative to crown clades in the Kuraku et al., 2009), which is corroborated by a stem lineage to Gnathostomata. study of microRNAs and morphology (Heimberg et Jawed Vertebrates al., 2010) that identified four unique microRNA families shared by hagfishes and lampreys, and so The phylogeny of Gnathostomata (Figure 3), resuscitated Cyclostomata (specifically, morpho- the jawed vertebrates, has been revised substan- logical data are indecisive on the question of tially, especially with regard to extinct groups. Liv- 3 BENTON ET AL.: ANIMAL HISTORY TIMESCALE pelmatozoan ossicles Echinodermata Eleutherozoa (12, 13) 515.5 (14) 509 Stromatocystites walcotti Ambulacraria Crinoidea Hemichordata Pterobranchia (15) 504.5 Rhabdotubus johanssoni Deuterostomia Enteropneusta Cephalochordata Tunicata Haikouichthys ercaicunensis Chordata Cyclostomata Petromyzontida Olfactores (19) 358.5 Vertebrata (16, 17) 514 Priscomyzon
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