title: Ancient proteins resolve the evolutionary history of Darwin's South American ungulates.
abstract: No large group of recently extinct placental mammals remains as evolutionarily cryptic as the approximately 280 genera grouped as 'South American native ungulates'. To Charles Darwin, who first collected their remains, they included perhaps the 'strangest animal[s] ever discovered'. Today, much like 180 years ago, it is no clearer whether they had one origin or several, arose before or after the Cretaceous/Palaeogene transition 66.2 million years ago, or are more likely to belong with the elephants and sirenians of superorder Afrotheria than with the euungulates (cattle, horses, and allies) of superorder Laurasiatheria. Morphology-based analyses have proved unconvincing because convergences are pervasive among unrelated ungulate-like placentals. Approaches using ancient DNA have also been unsuccessful, probably because of rapid DNA degradation in semitropical and temperate deposits. Here we apply proteomic analysis to screen bone samples of the Late Quaternary South American native ungulate taxa Toxodon (Notoungulata) and Macrauchenia (Litopterna) for phylogenetically informative protein sequences. For each ungulate, we obtain approximately 90% direct sequence coverage of type I collagen α1- and α2-chains, representing approximately 900 of 1,140 amino-acid residues for each subunit. A phylogeny is estimated from an alignment of these fossil sequences with collagen (I) gene transcripts from available mammalian genomes or mass spectrometrically derived sequence data obtained for this study. The resulting consensus tree agrees well with recent higher-level mammalian phylogenies. Toxodon and Macrauchenia form a monophyletic group whose sister taxon is not Afrotheria or any of its constituent clades as recently claimed, but instead crown Perissodactyla (horses, tapirs, and rhinoceroses). These results are consistent with the origin of at least some South American native ungulates from 'condylarths', a paraphyletic assembly of archaic placentals. With ongoing improvements in instrumentation and analytical procedures, proteomics may produce a revolution in systematics such as that achieved by genomics, but with the possibility of reaching much further back in time.
authors: 1] BioArCh, University of York, York YO10 5DD, UK [2] Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.
authors: Frido
authors: F
authors: Welker
authors: BioArCh, University of York, York YO10 5DD, UK.
authors: Matthew J
authors: MJ
authors: Collins
authors: BioArCh, University of York, York YO10 5DD, UK.
authors: Jessica A
authors: JA
authors: Thomas
authors: BioArCh, University of York, York YO10 5DD, UK.
authors: Marc
authors: M
authors: Wadsley
authors: Department of Earth Sciences, Natural History Museum, London SW7 5BD, UK.
authors: Selina
authors: S
authors: Brace
authors: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark.
authors: Enrico
authors: E
authors: Cappellini
authors: Institute of Zoology, Zoological Society of London, London NW1 4RY, UK.
authors: Samuel T
authors: ST
authors: Turvey
authors: CONICET- División Paleontología de Vertebrados, Museo de La Plata. Facultad de Ciencias Naturales y Museo de La Plata, Universidad Nacional de La Plata. Paseo del Bosque s/n, B1900FWA, La Plata, Argentina.
authors: Marcelo
authors: M
authors: Reguero
authors: CONICET- División Paleontología de Vertebrados, Museo de La Plata. Facultad de Ciencias Naturales y Museo de La Plata, Universidad Nacional de La Plata. Paseo del Bosque s/n, B1900FWA, La Plata, Argentina.
authors: Javier N
authors: JN
authors: Gelfo
authors: Sección Paleontología de Vertebrados. Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", 470 Angel Gallardo Av., C1405DJR, Buenos Aires, Argentina.
authors: Alejandro
authors: A
authors: Kramarz
authors: Institute of Anthropology, Johannes Gutenberg-University, Anselm-Franz-von-Bentzel-Weg 7, D-55128 Mainz, Germany.
authors: Joachim
authors: J
authors: Burger
authors: Department of Chemistry, University of York, York YO10 5DD, UK.
authors: Jane
authors: J
authors: Thomas-Oates
authors: Bioscience Technology Facility, Department of Biology, University of York, York YO10 5DD, UK.
authors: David A
authors: DA
authors: Ashford
authors: Bioscience Technology Facility, Department of Biology, University of York, York YO10 5DD, UK.
authors: Peter D
authors: PD
authors: Ashton
authors: BioArCh, University of York, York YO10 5DD, UK.
authors: Keri
authors: K
authors: Rowsell
authors: Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA.
authors: Duncan M
authors: DM
authors: Porter
authors: Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK.
authors: Benedikt
authors: B
authors: Kessler
authors: Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FZ, UK.
authors: Roman
authors: R
authors: Fischer
authors: Applications Development, Bruker Daltonik GmbH, 28359 Bremen, Germany.
authors: Carsten
authors: C
authors: Baessmann
authors: Applications Development, Bruker Daltonik GmbH, 28359 Bremen, Germany.
authors: Stephanie
authors: S
authors: Kaspar
authors: Novo Nordisk Foundation Center for Protein Research, Faculty of Health Sciences, University of Copenhagen, Blegdamsvej 3b, 2200 Copenhagen, Denmark.
authors: Jesper V
authors: JV
authors: Olsen
authors: Department of Materials Science and Metallurgy, University of Cambridge, Cambridge CB3 0FS, UK.
authors: Patrick
authors: P
authors: Kiley
authors: Department of Materials Science and Metallurgy, University of Cambridge, Cambridge CB3 0FS, UK.
authors: James A
authors: JA
authors: Elliott
authors: Novo Nordisk Foundation Center for Protein Research, Faculty of Health Sciences, University of Copenhagen, Blegdamsvej 3b, 2200 Copenhagen, Denmark.
authors: Christian D
authors: CD
authors: Kelstrup
authors: Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland.
authors: Victoria
authors: V
authors: Mullin
authors: 1] BioArCh, University of York, York YO10 5DD, UK [2] Institute for Biochemistry and Biology, Karl-Liebknecht-Strasse 24-25, 14476 Potsdam OT Golm, Germany.
authors: Michael
authors: M
authors: Hofreiter
authors: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark.
authors: Eske
authors: E
authors: Willerslev
authors: Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.
authors: Jean-Jacques
authors: JJ
authors: Hublin
authors: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark.
authors: Ludovic
authors: L
authors: Orlando
authors: Department of Earth Sciences, Natural History Museum, London SW7 5BD, UK.
authors: Ian
authors: I
authors: Barnes
authors: Department of Mammalogy, American Museum of Natural History, New York, New York 10024, USA.
authors: Ross D E
authors: RD
authors: MacPhee
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001842:Bone and Bones / Q000737:chemistry; D002417:Cattle; D024042:Collagen Type I / Q000737:chemistry* / Q000235:genetics; D005260:Female; D005580:Fossils; D008322:Mammals / Q000145:classification*; D010527:Perissodactyla / Q000145:classification; D010802:Phylogeny; D010920:Placenta; D011247:Pregnancy; D040901:Proteomics; D013020:South America
chemical_list: D024042:Collagen Type I