Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species

Nater A 1 , Mattle-Greminger MP 2 , Nurcahyo A 3 , Nowak MG 4 , de Manuel M 5 , Desai T 6 Show all authors , Groves C 3 , Pybus M 5 , Sonay TB 7 , Roos C 8 , Lameira AR 9 , Wich SA 10 , Askew J 11 , Davila-Ross M 12 , Fredriksson G 13 , de Valles G 5 , Casals F 14 , Prado-Martinez J 15 , Goossens B 16 , Verschoor EJ 17 , Warren KS 18 , Singleton I 19 , Marques DA 20 , Pamungkas J 21 , Perwitasari-Farajallah D 22 , Rianti P 23 , Tuuga A 24 , Gut IG 25 , Gut M 25 , Orozco-terWengel P 26 , van Schaik CP 7 , Bertranpetit J 27 , Anisimova M 28 , Scally A 6 , Marques-Bonet T 29 , Meijaard E 30 , Krützen M 31

Affiliations 

  • 1 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland; Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland; Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, 78457 Konstanz, Germany. Electronic address: alexander.nater@uzh.ch
  • 2 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland; Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
  • 3 School of Archaeology and Anthropology, Australian National University, Canberra, ACT, Australia
  • 4 Sumatran Orangutan Conservation Programme (PanEco-YEL), Jalan Wahid Hasyim 51/74, Medan 20154, Indonesia; Department of Anthropology, Southern Illinois University, 1000 Faner Drive, Carbondale, IL 62901, USA
  • 5 Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, Doctor Aiguader 88, Barcelona 08003, Spain
  • 6 Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK
  • 7 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
  • 8 Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, 37077 Göttingen, Germany
  • 9 Department of Anthropology, Durham University, Dawson Building, South Road, Durham DH1 3LE, UK; School of Psychology & Neuroscience, St. Andrews University, St. Mary's Quad, South Street, St. Andrews, Fife KY16 9JP, Scotland, UK
  • 10 School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool L3 3AF, UK; Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, Amsterdam 1098, the Netherlands
  • 11 Department of Biological Sciences, University of Southern California, 3616 Trousdale Parkway, Los Angeles, CA 90089, USA
  • 12 Department of Psychology, University of Portsmouth, King Henry Building, King Henry 1(st) Street, Portsmouth PO1 2DY, UK
  • 13 Sumatran Orangutan Conservation Programme (PanEco-YEL), Jalan Wahid Hasyim 51/74, Medan 20154, Indonesia; Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, Amsterdam 1098, the Netherlands
  • 14 Servei de Genòmica, Universitat Pompeu Fabra, Doctor Aiguader 88, Barcelona 08003, Spain
  • 15 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, UK
  • 16 School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK; Danau Girang Field Centre, c/o Sabah Wildlife Department, Wisma Muis, 88100 Kota Kinabalu, Sabah, Malaysia; Sabah Wildlife Department, Wisma Muis, 88100 Kota Kinabalu, Sabah, Malaysia; Sustainable Places Research Institute, Cardiff University, 33 Park Place, Cardiff CF10 3BA, UK
  • 17 Department of Virology, Biomedical Primate Research Centre, Lange Kleiweg 161, 2288GJ Rijswijk, the Netherlands
  • 18 Conservation Medicine Program, College of Veterinary Medicine, Murdoch University, South Street, Murdoch, WA 6150, Australia
  • 19 Sumatran Orangutan Conservation Programme (PanEco-YEL), Jalan Wahid Hasyim 51/74, Medan 20154, Indonesia; Foundation for a Sustainable Ecosystem (YEL), Medan, Indonesia
  • 20 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland; Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerland
  • 21 Primate Research Center, Bogor Agricultural University, Bogor 16151, Indonesia; Faculty of Veterinary Medicine, Bogor Agricultural University, Darmaga Campus, Bogor 16680, Indonesia
  • 22 Primate Research Center, Bogor Agricultural University, Bogor 16151, Indonesia; Animal Biosystematics and Ecology Division, Department of Biology, Bogor Agricultural University, Jalan Agatis, Dramaga Campus, Bogor 16680, Indonesia
  • 23 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland; Primate Research Center, Bogor Agricultural University, Bogor 16151, Indonesia; Animal Biosystematics and Ecology Division, Department of Biology, Bogor Agricultural University, Jalan Agatis, Dramaga Campus, Bogor 16680, Indonesia
  • 24 Sabah Wildlife Department, Wisma Muis, 88100 Kota Kinabalu, Sabah, Malaysia
  • 25 CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, Barcelona 08028, Spain; Universitat Pompeu Fabra (UPF), Plaça de la Mercè 10, 08002 Barcelona, Spain
  • 26 School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK
  • 27 Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, Doctor Aiguader 88, Barcelona 08003, Spain; Leverhulme Centre for Human Evolutionary Studies, Department of Archaeology and Anthropology, University of Cambridge, Cambridge, UK
  • 28 Institute of Applied Simulations, School of Life Sciences and Facility Management, Zurich University of Applied Sciences (ZHAW), Einsiedlerstrasse 31a, 8820 Wädenswil, Switzerland; Swiss Institute of Bioinformatics, Quartier Sorge-Batiment Genopode, 1015 Lausanne, Switzerland
  • 29 Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, Doctor Aiguader 88, Barcelona 08003, Spain; CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, Barcelona 08028, Spain; Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona 08010, Spain
  • 30 School of Archaeology and Anthropology, Australian National University, Canberra, ACT, Australia; Borneo Futures, Bandar Seri Begawan, Brunei Darussalam. Electronic address: emeijaard@gmail.com
  • 31 Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland. Electronic address: michael.kruetzen@aim.uzh.ch
Curr Biol, 2017 Nov 20;27(22):3487-3498.e10.
PMID: 29103940 DOI: 10.1016/j.cub.2017.09.047

Abstract

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.

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