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      Historical biogeography of the leopard ( Panthera pardus) and its extinct Eurasian populations

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          Abstract

          Background

          Resolving the historical biogeography of the leopard (Panthera pardus) is a complex issue, because patterns inferred from fossils and from molecular data lack congruence. Fossil evidence supports an African origin, and suggests that leopards were already present in Eurasia during the Early Pleistocene. Analysis of DNA sequences however, suggests a more recent, Middle Pleistocene shared ancestry of Asian and African leopards. These contrasting patterns led researchers to propose a two-stage hypothesis of leopard dispersal out of Africa: an initial Early Pleistocene colonisation of Asia and a subsequent replacement by a second colonisation wave during the Middle Pleistocene. The status of Late Pleistocene European leopards within this scenario is unclear: were these populations remnants of the first dispersal, or do the last surviving European leopards share more recent ancestry with their African counterparts?

          Results

          In this study, we generate and analyse mitogenome sequences from historical samples that span the entire modern leopard distribution, as well as from Late Pleistocene remains. We find a deep bifurcation between African and Eurasian mitochondrial lineages (~ 710 Ka), with the European ancient samples as sister to all Asian lineages (~ 483 Ka). The modern and historical mainland Asian lineages share a relatively recent common ancestor (~ 122 Ka), and we find one Javan sample nested within these.

          Conclusions

          The phylogenetic placement of the ancient European leopard as sister group to Asian leopards suggests that these populations originate from the same out-of-Africa dispersal which founded the Asian lineages. The coalescence time found for the mitochondrial lineages aligns well with the earliest undisputed fossils in Eurasia, and thus encourages a re-evaluation of the identification of the much older putative leopard fossils from the region. The relatively recent ancestry of all mainland Asian leopard lineages suggests that these populations underwent a severe population bottleneck during the Pleistocene. Finally, although only based on a single sample, the unexpected phylogenetic placement of the Javan leopard could be interpreted as evidence for exchange of mitochondrial lineages between Java and mainland Asia, calling for further investigation into the evolutionary history of this subspecies.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-018-1268-0) contains supplementary material, which is available to authorized users.

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          Most cited references50

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          A high-coverage genome sequence from an archaic Denisovan individual.

          We present a DNA library preparation method that has allowed us to reconstruct a high-coverage (30×) genome sequence of a Denisovan, an extinct relative of Neandertals. The quality of this genome allows a direct estimation of Denisovan heterozygosity indicating that genetic diversity in these archaic hominins was extremely low. It also allows tentative dating of the specimen on the basis of "missing evolution" in its genome, detailed measurements of Denisovan and Neandertal admixture into present-day human populations, and the generation of a near-complete catalog of genetic changes that swept to high frequency in modern humans since their divergence from Denisovans.
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            Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations

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              Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA.

              This protocol describes a method for converting short single-stranded and double-stranded DNA into libraries compatible with high-throughput sequencing using Illumina technology. This method has primarily been developed to improve sequence retrieval from ancient DNA, but it is also applicable to the sequencing of short or degraded DNA from other sources, and it can also be used for sequencing oligonucleotides. Single-stranded library preparation is performed by ligating a biotinylated adapter oligonucleotide to the 3' ends of heat-denatured DNA. The resulting strands are then immobilized on streptavidin-coated beads and copied with a polymerase. A second adapter is attached by blunt-end ligation, and library preparation is completed by PCR amplification. We estimate that intact DNA strands are recovered in the library with ∼50% efficiency. Libraries can be generated from up to 12 DNA or oligonucleotide samples in parallel within 2 d.
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                Author and article information

                Contributors
                paijmans.jla@gmail.com
                axel.barlow.ab@gmail.com
                dwgfoerster@gmail.com
                kihenneb@uni-potsdam.de
                mmeyer@eva.mpg.de
                nickel@eva.mpg.de
                doris.nagel@univie.ac.at
                rasmushav@gmail.com
                gennady.baryshnikov@zin.ru
                u.joger@3landesmuseen.de
                wilfried.rosendahl@mannheim.de
                michi@palaeo.eu
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                23 October 2018
                23 October 2018
                2018
                : 18
                : 156
                Affiliations
                [1 ]ISNI 0000 0001 0942 1117, GRID grid.11348.3f, Institute for Biochemistry and Biology, , University of Potsdam, ; Karl-Liebknecht-Straße 24–25, 14476 Potsdam, Germany
                [2 ]ISNI 0000 0001 0708 0355, GRID grid.418779.4, Leibniz Institute for Zoo- and Wildlife Research, ; Alfred-Kowalke-Strasse 17, 10315 Berlin, Germany
                [3 ]ISNI 0000 0001 2159 1813, GRID grid.419518.0, Department of Evolutionary Genetics, , Max Planck Institute for Evolutionary Anthropology, ; Deutscher Platz 6, 04103 Leipzig, Germany
                [4 ]ISNI 0000 0001 2286 1424, GRID grid.10420.37, Institute for Paleontology, , University of Vienna, ; Althanstrasse 14, Vienna, A-1090 Austria
                [5 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Natural History Museum of Denmark, , University of Copenhagen, ; Øster Voldgade 5–7, Copenhagen, Denmark
                [6 ]ISNI 0000 0001 2314 7601, GRID grid.439287.3, Zoological Institute, Russian Academy of Sciences, ; Universitetskaya Naberezhnaya 1, 199034 St. Petersburg, Russia
                [7 ]ISNI 0000 0001 2227 9098, GRID grid.462857.a, State Natural History Museum, ; Pockelsstr. 10, 38106 Braunschweig, Germany
                [8 ]GRID grid.461611.5, Reiss-Engelhorn Museen and Curt-Engelhorn-Centre for Archaeometry, ; C4 8, 68159 Mannheim, Germany
                Author information
                http://orcid.org/0000-0002-1938-7052
                Article
                1268
                10.1186/s12862-018-1268-0
                6198532
                30348080
                0da6990d-5a2b-4539-a0fb-b7b3dbf1cd7d
                © The Author(s). 2018

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 16 February 2018
                : 26 September 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 310763
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100007065, Nvidia;
                Award ID: Academic Hardware Grant
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Evolutionary Biology
                ancient dna,hybridisation capture,leopards,mitochondrial genomes,mitogenomes,mtdna,palaeogenetics,panthera pardus

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