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The Evolutionary History of Neanderthal and Denisovan Y The evolutionary history of Neanderthal and Denisovan Y chromosomes Martin Petr, Mateja Hajdinjak, Qiaomei Fu, Elena Essel, Hélène Rougier, Isabelle Crevecoeur, Patrick Semal, V Liubov, Vladimir Doronichev, Carles Lalueza-Fox, et al. To cite this version: Martin Petr, Mateja Hajdinjak, Qiaomei Fu, Elena Essel, Hélène Rougier, et al.. The evolution- ary history of Neanderthal and Denisovan Y chromosomes. Science, American Association for the Advancement of Science, 2020. hal-02990265 HAL Id: hal-02990265 https://hal.archives-ouvertes.fr/hal-02990265 Submitted on 5 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. RESEARCH ◥ male late Neanderthals, Spy 94a (38 to 39 ka old) REPORT and Mezmaiskaya 2 (43 to 45 ka old) (13) (Fig. 1A). To enrich for Y chromosome DNA F1 YEVOLUTION from these individuals, we performed hybrid- ization capture using probes we designed to The evolutionary history of Neanderthal target ~6.9 Mb of the nonrecombining portion of the human Y chromosome (Fig. 1B) (14). and Denisovan Y chromosomes This yielded sequence coverage of 1.4× for Denisova 4, 3.5× for Denisova 8, 0.8× for Spy Martin Petr1*,MatejaHajdinjak1,2,QiaomeiFu3,4,5,ElenaEssel1,HélèneRougier6,IsabelleCrevecoeur7, 94a, and 14.3× for Mezmaiskaya 2 (Fig. 1C Patrick Semal8, Liubov V. Golovanova9, Vladimir B. Doronichev9, Carles Lalueza-Fox10, and table S2). In addition, we used a capture Marco de la Rasilla11, Antonio Rosas12, Michael V. Shunkov13, Maxim B. Kozlikin13, array designed for modern human Y chro- Anatoli P. Derevianko13, Benjamin Vernot1, Matthias Meyer1, Janet Kelso1* mosomes (3)toobtain7.9× coverage of ~560 kb of the Y chromosome from the ~46- to Ancient DNA has allowed the study of human history in previously unseen detail. However, we lack 53-ka-old El Sidrón 1253 Neanderthal (Fig. 1C comprehensive studies of the Y chromosomes of Denisovans and Neanderthals. Sequencing Y and table S2), which has been analyzed pre- chromosomes from two Denisovans and three Neanderthals shows that the Y chromosomes of viously (15, 16). Denisovans split around 700 thousand years ago from a lineage shared by Neanderthals and modern To call genotypes of the captured archaic hu- human Y chromosomes, which diverged from each other around 370 thousand years ago. The man and previously published modern human phylogenetic relationships of archaic and modern human Y chromosomes differ from the population Ychromosomes(4, 17, 18), we leveraged the relationships inferred from the autosomal genomes and mirror mitochondrial DNA phylogenies, haploid nature of the human Y chromosome indicating replacement of both the mitochondrial and Y chromosomal gene pools in late Neanderthals. and implemented a consensus approach that This replacement is plausible if the low effective population size of Neanderthals resulted in an increased requires at least 90% of the reads observed at genetic load in Neanderthals relative to modern humans. each site covered by at least three reads to agree on a single allele (14). This minimizes the im- pact of aDNA damage on genotyping accuracy ncient DNA (aDNA) has transformed our and Y chromosomes sampled from two pop- while allowing for a small amount of sequenc- understanding of human evolutionary ulations provide an upper bound for the last ing error or contamination (fig. S8) (14). history, revealing complex patterns of time they experienced gene flow. To determine the relationships between population migration and gene flow, in- The mtDNA and autosomal sequences of Denisovan, Neanderthal, and modern human A cluding admixture from archaic humans Neanderthals, Denisovans, and modern humans Y chromosomes, we constructed a neighbor- into modern humans. Particularly important have revealed puzzling phylogenetic discrep- joining tree from the Y chromosome geno- have been analyses of autosomal sequences ancies. Autosomal genomes show that Nean- type calls (14). Unlike the rest of the nuclear (1, 2), which represent a composite of geneal- derthals and Denisovans are sister groups genome, which puts Denisovans and Nean- ogies of any individual’sancestors.Although that split from modern humans between derthals as sister groups to modern humans (2), mitochondrial DNA (mtDNA) and Y chromo- 550 thousand and 765 thousand years (ka) ago the Denisovan Y chromosomes form a separate somes only provide information about single (6). By contrast, the mtDNAs of Neanderthals lineage that split before Neanderthal and mod- maternal and paternal lineages, they offer a and modern humans are more similar to one ern human Y chromosomes diverged from each distinctive perspective on various aspects of another [time to the most recent common other (Fig. 2A). Notably, all three late Neander- F2 population history such as sex-specific migra- ancestor (TMRCA) of 360 to 468 ka ago] than thal Y chromosomes cluster together and fall tion, matrilocality and patrilocality, and variance to the mtDNAs of Denisovans (7). Notably, outside of the variation of present-day human in reproductive success between individuals ~400-ka-old early Neanderthals from Sima de Ychromosomes[Fig.2A;(10)]. (3–5). Furthermore, because of their lower ef- los Huesos were shown to carry mitochon- To estimate the TMRCA of archaic and mod- fective population size (Ne)comparedwiththat drial genomes related to Denisovan mtDNAs ern human Y chromosomes, we adapted a of autosomal loci, coalescent times of mtDNA (8, 9). This suggests that Neanderthals origi- previously published method that calculates nally carried a Denisovan-like mtDNA, which the archaic-modern human TMRCA as a pro- 1Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany. 2The was later completely replaced through ancient portion of the deepest known split in present- Francis Crick Institute, NW1 1AT London, UK. 3Key Laboratory gene flow from an early lineage related to day human Y variation (4, 10, 14)andistherefore of Vertebrate Evolution and Human Origins of Chinese modern humans (7, 9). robust to low coverage and aDNA damage (10) Academy of Sciences, IVPP, CAS, Beijing 100044, China. 4CAS Center for Excellence in Life and Paleoenvironment, Beijing The Y chromosomes of Neanderthals and (fig. S8 and table S2). We first calculated the 100044, China. 5University of Chinese Academy of Sciences, Denisovans should provide an additional source mutation rate in the 6.9-Mb target region to be Beijing 100049, China. 6Department of Anthropology, California of information about population splits and 7.34 × 10−10 per base pair per year [bootstrap State University, Northridge, Northridge, CA 91330-8244, USA. −10 7Université de Bordeaux, CNRS, UMR 5199-PACEA, 33615 gene flow events between archaic and mod- confidence interval (CI) 6.27 × 10 to 8.46 × −10 Pessac Cedex, France. 8Royal Belgian Institute of Natural ern humans or populations related to them. 10 ] (fig. S11 and table S11) (14) and used it Sciences, 1000 Brussels, Belgium. 9ANO Laboratory of However, with the exception of a small to estimate a TMRCA of ~249 ka ago (boot- Prehistory 14 Linia 3-11, St. Petersburg 1990 34, Russia. amount of Neanderthal Y chromosome cod- strap CI 213 to 293 ka ago) (fig. S11 and table 10Institute of Evolutionary Biology, Consejo Superior de Investigaciones Científicas, Universitat Pompeu Fabra, 08003 ing sequence (118 kb) (10), none of the male S11) (14) for the African A00 lineage and a set Barcelona, Spain. 11Área de Prehistoria, Departamento de Neanderthals or Denisovans studied to date of non-African Y chromosomes (4, 18). This is Historia, Universidad de Oviedo, 33011 Oviedo, Spain. have yielded sufficient amounts of endoge- consistent with other studies of present-day 12Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, nous DNA to allow comprehensive studies of human Y chromosomes (4, 17), suggesting that 28006 Madrid, Spain. 13Institute of Archaeology and archaic human Y chromosomes. the Y chromosomal regions we sequenced are Ethnography, Siberian Branch, Russian Academy of Sciences, Previous genetic studies identified two male not unusual in terms of their mutation rate. Novosibirsk, Russia. *Corresponding author. Email: [email protected] (M.P.); kelso@ Denisovans, Denisova 4 (55 to 84 ka old) and We then used this A00 divergence time of eva.mpg.de (J.K.) Denisova 8 (106 to 136 ka old) (11, 12), and two 249 ka ago to infer TMRCAs between archaic SCIENCE sciencemag.org 00 MONTH 2020 • VOL 000 ISSUE 0000 1 MS no: REabb6460/AB/EVOLUTION, MOLEC BIOL RESEARCH | REPORT A Denisova 8 Denisova 4 El Sidrón 1253 Mezmaiskaya 2 Spy 94a 150 125 100 75 50 0 age [ka ago] 0 Mb 10 Mb 20 Mb 30 Mb B ampliconic X−degenerate heterochromatic X−transposed pseudo−autosomal others C 20X Denisova 4 10X 2X 20X Denisova 8 10X 2X 20X Spy 94a 10X 2X 20X Mezmaiskaya 2 10X 2X El Sidrón 1253 20X 10X (560 kb) 2X 0X 5X 10X 15X 20X 25X coverage per site Fig. 1. Overview of male archaic humans in our study. (A)Archaeologicalsitelocations.Agesofspecimensareshownasaninset(12,
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