title: Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus.
abstract: Recent genomic data have revealed multiple interactions between Neanderthals and modern humans, but there is currently little genetic evidence regarding Neanderthal behaviour, diet, or disease. Here we describe the shotgun-sequencing of ancient DNA from five specimens of Neanderthal calcified dental plaque (calculus) and the characterization of regional differences in Neanderthal ecology. At Spy cave, Belgium, Neanderthal diet was heavily meat based and included woolly rhinoceros and wild sheep (mouflon), characteristic of a steppe environment. In contrast, no meat was detected in the diet of Neanderthals from El Sidrón cave, Spain, and dietary components of mushrooms, pine nuts, and moss reflected forest gathering. Differences in diet were also linked to an overall shift in the oral bacterial community (microbiota) and suggested that meat consumption contributed to substantial variation within Neanderthal microbiota. Evidence for self-medication was detected in an El Sidrón Neanderthal with a dental abscess and a chronic gastrointestinal pathogen (Enterocytozoon bieneusi). Metagenomic data from this individual also contained a nearly complete genome of the archaeal commensal Methanobrevibacter oralis (10.2× depth of coverage)-the oldest draft microbial genome generated to date, at around 48,000 years old. DNA preserved within dental calculus represents a notable source of information about the behaviour and health of ancient hominin specimens, as well as a unique system that is useful for the study of long-term microbial evolution.
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Laura S
authors.initials: LS
authors.lastname: Weyrich
authors.affiliation: Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, University of Sydney, Sydney, Australia.
authors.forename: Sebastian
authors.initials: S
authors.lastname: Duchene
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Julien
authors.initials: J
authors.lastname: Soubrier
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Luis
authors.initials: L
authors.lastname: Arriola
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Bastien
authors.initials: B
authors.lastname: Llamas
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: James
authors.initials: J
authors.lastname: Breen
authors.affiliation: Department of Human Biology, University of Cape Town, Cape Town, South Africa.
authors.forename: Alan G
authors.initials: AG
authors.lastname: Morris
authors.affiliation: Danube Private University, Krems, Austria.|State Office for Heritage Management and Archaeology, Saxony-Anhalt, Germany.|Heritage Museum, Halle, Germany.|Institute for Prehistory and Archaeological Science, Basel University, Switzerland.
authors.forename: Kurt W
authors.initials: KW
authors.lastname: Alt
authors.affiliation: Department of Biology, University of Florence, Florence, Italy.
authors.forename: David
authors.initials: D
authors.lastname: Caramelli
authors.affiliation: State Office for Heritage Management and Archaeology, Saxony-Anhalt, Germany.|Heritage Museum, Halle, Germany.
authors.forename: Veit
authors.initials: V
authors.lastname: Dresely
authors.affiliation: Human Origins and Palaeo Environments Group, Oxford Brookes University, Oxford, UK.
authors.forename: Milly
authors.initials: M
authors.lastname: Farrell
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Andrew G
authors.initials: AG
authors.lastname: Farrer
authors.affiliation: Paleoanthropology, Senckenberg Centre for Human Evolution and Paleoenvironments, Eberhard Karls University of Tübingen, Tübingen, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Francken
authors.affiliation: School of Dentistry, The University of Adelaide, Adelaide, Australia.
authors.forename: Neville
authors.initials: N
authors.lastname: Gully
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Haak
authors.affiliation: Catalan Institution for Research and Advanced Studies (ICREA), Pg Lluís Companys 23, 08010 Barcelona, Catalonia, Spain.|Departament de Prehistòria, Facultat de Filosofia i Lletres, Universitat Autònoma de Barcelona, Barcelona, Catalonia, Spain.
authors.forename: Karen
authors.initials: K
authors.lastname: Hardy
authors.affiliation: Paleoanthropology, Senckenberg Centre for Human Evolution and Paleoenvironments, Eberhard Karls University of Tübingen, Tübingen, Germany.
authors.forename: Katerina
authors.initials: K
authors.lastname: Harvati
authors.affiliation: Institute of Anthropology, University of Mainz, Mainz, Germany.
authors.forename: Petra
authors.initials: P
authors.lastname: Held
authors.affiliation: Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, University of Sydney, Sydney, Australia.
authors.forename: Edward C
authors.initials: EC
authors.lastname: Holmes
authors.affiliation: School of Dentistry, The University of Adelaide, Adelaide, Australia.
authors.forename: John
authors.initials: J
authors.lastname: Kaidonis
authors.affiliation: Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain.
authors.forename: Carles
authors.initials: C
authors.lastname: Lalueza-Fox
authors.affiliation: Área de Prehistoria, Departamento de Historia, Universidad de Oviedo, Oviedo, Spain.
authors.forename: Marco
authors.initials: M
authors.lastname: de la Rasilla
authors.affiliation: Paleoanthropology Group, Department of Paleobiology, Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain.
authors.forename: Antonio
authors.initials: A
authors.lastname: Rosas
authors.affiliation: Scientific Service Heritage, Royal Belgian Institute of Natural Sciences, Brussels, Belgium.
authors.forename: Patrick
authors.initials: P
authors.lastname: Semal
authors.affiliation: Department of Bioarchaeology, Institute of Archaeology, University of Warsaw, Warsaw, Poland.
authors.forename: Arkadiusz
authors.initials: A
authors.lastname: Soltysiak
authors.affiliation: School of Dentistry, The University of Adelaide, Adelaide, Australia.
authors.forename: Grant
authors.initials: G
authors.lastname: Townsend
authors.affiliation: Istituto Italiano per l'Africa e l'Oriente (IsIAO), Rome, Italy.
authors.forename: Donatella
authors.initials: D
authors.lastname: Usai
authors.affiliation: State Office for Cultural Heritage Management Baden-Württemberg, Esslingen, Germany.
authors.forename: Joachim
authors.initials: J
authors.lastname: Wahl
authors.affiliation: Department of Algorithms in Bioinformatics, University of Tübingen, Tübingen, Germany.
authors.forename: Daniel H
authors.initials: DH
authors.lastname: Huson
authors.affiliation: Department of Archaeology, Classics and Egyptology, School of Histories, Languages and Cultures, University of Liverpool, Liverpool, UK.|Department of Archaeology, University of Aberdeen, Aberdeen, UK.|Department of Archaeology, Simon Fraser University, Burnaby, British Columbia, Canada.
authors.forename: Keith
authors.initials: K
authors.lastname: Dobney
authors.affiliation: Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.
authors.forename: Alan
authors.initials: A
authors.lastname: Cooper
mesh_terms: D000818:Animals; D001530:Belgium; D060435:Carnivory; D059552:Caves; D000072441:DNA, Ancient / Q000032:analysis*; D003728:Dental Calculus / Q000737:chemistry*; D004032:Diet / Q000266:history*; D021862:Enterocytozoon / Q000235:genetics / Q000302:isolation & purification; D005518:Food Preferences; D016680:Genome, Bacterial / Q000235:genetics; D006262:Health / Q000266:history*; D049690:History, Ancient; D006801:Humans; D007422:Intestines / Q000382:microbiology; D008460:Meat / Q000266:history; D041581:Methanobrevibacter / Q000235:genetics / Q000302:isolation & purification; D009055:Mouth / Q000382:microbiology; D059125:Neanderthals / Q000382:microbiology* / Q000523:psychology*; D002679:Pan troglodytes / Q000382:microbiology; D010407:Penicillium / Q000737:chemistry; D010527:Perissodactyla; D012756:Sheep; D013030:Spain; D013270:Stomach / Q000382:microbiology; D013559:Symbiosis; D013997:Time Factors; D000066988:Vegetarians / Q000266:history
chemical_list: D000072441:DNA, Ancient