Home LiteratureArticle Details
PMID: 29967444 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Adaptation and conservation insights from the koala genome.

Nature genetics ·Vol. 50 ·No. 8 ·2018-00-00 ·Pages 1102-1111

Johnson RN, O'Meally D, Chen Z, Etherington GJ, Ho SYW, Nash WJ, Grueber CE, Cheng Y, Whittington CM, Dennison S, Peel E, Haerty W, O'Neill RJ, Colgan D, Russell TL, Alquezar-Planas DE, Attenbrow V, Bragg JG, Brandies PA, Chong AY, Deakin JE, Di Palma F, Duda Z, Eldridge MDB, Ewart KM, Hogg CJ, Frankham GJ, Georges A, Gillett AK, Govendir M, Greenwood AD, Hayakawa T, Helgen KM, Hobbs M, Holleley CE, Heider TN, Jones EA, King A, Madden D, Graves JAM, Morris KM, Neaves LE, Patel HR, Polkinghorne A, Renfree MB, Robin C, Salinas R, Tsangaras K, Waters PD, Waters SA, Wright B, Wilkins MR, Timms P, Belov K

Abstract

The koala, the only extant species of the marsupial family Phascolarctidae, is classified as 'vulnerable' due to habitat loss and widespread disease. We sequenced the koala genome, producing a complete and contiguous marsupial reference genome, including centromeres. We reveal that the koala's ability to detoxify eucalypt foliage may be due to expansions within a cytochrome P450 gene family, and its ability to smell, taste and moderate ingestion of plant secondary metabolites may be due to expansions in the vomeronasal and taste receptors. We characterized novel lactation proteins that protect young in the pouch and annotated immune genes important for response to chlamydial disease. Historical demography showed a substantial population crash coincident with the decline of Australian megafauna, while contemporary populations had biogeographic boundaries and increased inbreeding in populations affected by historic translocations. We identified genetically diverse populations that require habitat corridors and instituting of translocation programs to aid the koala's survival in the wild.

MeSH Terms
Adaptation, Physiological/genetics Animals Australia Chlamydia Infections/genetics Cytochrome P-450 Enzyme System/genetics,metabolism Female Genome Molecular Sequence Annotation/methods Phascolarctidae/genetics,metabolism Translocation, Genetic
Chemicals
Cytochrome P-450 Enzyme System
Authors & Affiliations
54 authors, click to expand affiliations / ORCID
Johnson Rebecca N ORCID
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia. [email protected]. | School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia. [email protected].
O'Meally Denis
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia. | Animal Research Centre, Faculty of Science, Health, Education & Engineering, University of the Sunshine Coast, Maroochydore, Queensland, Australia.
Chen Zhiliang
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Kensington, New South Wales, Australia.
Etherington Graham J
Earlham Institute, Norwich Research Park, Norwich, UK.
Ho Simon Y W ORCID
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Nash Will J
Earlham Institute, Norwich Research Park, Norwich, UK.
Grueber Catherine E ORCID
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia. | San Diego Zoo Global, San Diego, CA, USA.
Cheng Yuanyuan
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia. | UQ Genomics Initiative, University of Queensland, St Lucia, Queensland, Australia.
Whittington Camilla M
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Dennison Siobhan
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Peel Emma
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Haerty Wilfried
Earlham Institute, Norwich Research Park, Norwich, UK.
O'Neill Rachel J
Department of Molecular and Cell Biology and Institute for Systems Genomics, University of Connecticut, Storrs, CT, USA.
Colgan Don
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Russell Tonia L
Ramaciotti Centre for Genomics, University of New South Wales, Kensington, New South Wales, Australia.
Alquezar-Planas David E
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Attenbrow Val
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Bragg Jason G
Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia. | National Herbarium of New South Wales, Royal Botanic Gardens & Domain Trust, Sydney, New South Wales, Australia.
Brandies Parice A
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Chong Amanda Yoon-Yee
Earlham Institute, Norwich Research Park, Norwich, UK. | Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
Deakin Janine E
Institute for Applied Ecology, University of Canberra, Bruce, Australian Capital Territory, Australia.
Di Palma Federica
Earlham Institute, Norwich Research Park, Norwich, UK. | Department of Biological Sciences, University of East Anglia, Norwich, UK.
Duda Zachary
Department of Molecular and Cell Biology and Institute for Systems Genomics, University of Connecticut, Storrs, CT, USA.
Eldridge Mark D B
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Ewart Kyle M
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Hogg Carolyn J
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Frankham Greta J
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Georges Arthur
Institute for Applied Ecology, University of Canberra, Bruce, Australian Capital Territory, Australia.
Gillett Amber K
Australia Zoo Wildlife Hospital, Beerwah, Queensland, Australia.
Govendir Merran
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Greenwood Alex D
Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany. | Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.
Hayakawa Takashi
Department of Wildlife Science (Nagoya Railroad Co., Ltd.), Primate Research Institute, Kyoto University, Inuyama, Japan. | Japan Monkey Centre, Inuyama, Japan.
Helgen Kristofer M
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia. | School of Biological Sciences, Environment Institute, Centre for Applied Conservation Science, and ARC Centre of Excellence for Australian Biodiversity and Heritage, University of Adelaide, Adelaide, South Australia, Australia.
Hobbs Matthew ORCID
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Holleley Clare E
Australian National Wildlife Collection, National Research Collections Australia, CSIRO, Canberra, Australian Capital Territory, Australia.
Heider Thomas N
Department of Molecular and Cell Biology and Institute for Systems Genomics, University of Connecticut, Storrs, CT, USA.
Jones Elizabeth A
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
King Andrew
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia.
Madden Danielle
Animal Research Centre, Faculty of Science, Health, Education & Engineering, University of the Sunshine Coast, Maroochydore, Queensland, Australia.
Graves Jennifer A Marshall
Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia. | Institute for Applied Ecology, University of Canberra, Bruce, Australian Capital Territory, Australia. | School of Life Sciences, La Trobe University, Bundoora, Victoria, Australia.
Morris Katrina M
The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian, UK.
Neaves Linda E ORCID
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia. | Royal Botanic Garden Edinburgh, Edinburgh, UK.
Patel Hardip R
John Curtin School of Medical Research, Australian National University, Acton, Australian Capital Territory, Australia.
Polkinghorne Adam
Animal Research Centre, Faculty of Science, Health, Education & Engineering, University of the Sunshine Coast, Maroochydore, Queensland, Australia.
Renfree Marilyn B ORCID
School of BioSciences, University of Melbourne, Melbourne, Victoria, Australia.
Robin Charles ORCID
School of BioSciences, University of Melbourne, Melbourne, Victoria, Australia.
Salinas Ryan
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Kensington, New South Wales, Australia.
Tsangaras Kyriakos
Department of Translational Genetics, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus.
Waters Paul D
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Kensington, New South Wales, Australia.
Waters Shafagh A
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Kensington, New South Wales, Australia.
Wright Belinda
Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia. | School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
Wilkins Marc R
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Kensington, New South Wales, Australia. | Ramaciotti Centre for Genomics, University of New South Wales, Kensington, New South Wales, Australia.
Timms Peter
Faculty of Science, Health, Education & Engineering, University of the Sunshine Coast, Maroochydore, Queensland, Australia.
Belov Katherine
School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.
References (94)
94 references, click to expand
  1. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology.
    Bioinformatics. 2010 Oct 1;26(19):2455-7 PMID: 20671151
  2. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs.
    Bioinformatics. 2015 Oct 1;31(19):3210-2 PMID: 26059717
  3. The anatomy and histology of the nasal cavity of the koala (Phascolarctos cinereus).
    J Anat. 1984 Jan;138 ( Pt 1):55-65 PMID: 6706839
  4. Discovery of a novel retrovirus sequence in an Australian native rodent (Melomys burtoni): a putative link between gibbon ape leukemia virus and koala retrovirus.
    PLoS One. 2014 Sep 24;9(9):e106954 PMID: 25251014
  5. Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer.
    Cell. 2012 Feb 17;148(4):780-91 PMID: 22341448
  6. Climate sensitivity, sea level and atmospheric carbon dioxide.
    Philos Trans A Math Phys Eng Sci. 2013 Sep 16;371(2001):20120294 PMID: 24043864
  7. Characterisation of the immune compounds in koala milk using a combined transcriptomic and proteomic approach.
    Sci Rep. 2016 Oct 07;6:35011 PMID: 27713568
  8. Identification, characterisation and expression analysis of natural killer receptor genes in Chlamydia pecorum infected koalas (Phascolarctos cinereus).
    BMC Genomics. 2015 Oct 15;16:796 PMID: 26471184
  9. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid.
    Nature. 1998 May 7;393(6680):68-72 PMID: 9590690
  10. Degradation and remobilization of endogenous retroviruses by recombination during the earliest stages of a germ-line invasion.
    Proc Natl Acad Sci U S A. 2018 Aug 21;115(34):8609-8614 PMID: 30082403
  11. Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia.
    Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):4996-5001 PMID: 17360391
  12. UniProtKB/Swiss-Prot, the Manually Annotated Section of the UniProt KnowledgeBase: How to Use the Entry View.
    Methods Mol Biol. 2016;1374:23-54 PMID: 26519399
  13. Phylogeography of the Koala, (Phascolarctos cinereus), and Harmonising Data to Inform Conservation.
    PLoS One. 2016 Sep 02;11(9):e0162207 PMID: 27588685
  14. AUGUSTUS: ab initio prediction of alternative transcripts.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W435-9 PMID: 16845043
  15. Studies of the oestrous cycle, oestrus and pregnancy in the koala (Phascolarctos cinereus).
    J Reprod Fertil. 2000 Sep;120(1):49-57 PMID: 11006145
  16. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features.
    Bioinformatics. 2014 Apr 1;30(7):923-30 PMID: 24227677
  17. Long-read genome sequence assembly provides insight into ongoing retroviral invasion of the koala germline.
    Sci Rep. 2017 Nov 20;7(1):15838 PMID: 29158564
  18. Cytochrome P4502C9: an enzyme of major importance in human drug metabolism.
    Br J Clin Pharmacol. 1998 Jun;45(6):525-38 PMID: 9663807
  19. Plant secondary metabolites and vertebrate herbivores--from physiological regulation to ecosystem function.
    Curr Opin Plant Biol. 2005 Aug;8(4):430-5 PMID: 15939665
  20. The cytochrome p450 homepage.
    Hum Genomics. 2009 Oct;4(1):59-65 PMID: 19951895
  21. MAFFT multiple sequence alignment software version 7: improvements in performance and usability.
    Mol Biol Evol. 2013 Apr;30(4):772-80 PMID: 23329690
  22. Anchoring genome sequence to chromosomes of the central bearded dragon (Pogona vitticeps) enables reconstruction of ancestral squamate macrochromosomes and identifies sequence content of the Z chromosome.
    BMC Genomics. 2016 Jun 10;17:447 PMID: 27286959
  23. Full-length transcriptome assembly from RNA-Seq data without a reference genome.
    Nat Biotechnol. 2011 May 15;29(7):644-52 PMID: 21572440
  24. SARTools: A DESeq2- and EdgeR-Based R Pipeline for Comprehensive Differential Analysis of RNA-Seq Data.
    PLoS One. 2016 Jun 09;11(6):e0157022 PMID: 27280887
  25. The Vienna RNA websuite.
    Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W70-4 PMID: 18424795
  26. Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species.
    Biochem Syst Ecol. 2000 Nov 1;28(9):813-824 PMID: 10913843
  27. Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation.
    Nature. 2012 Jul 12;487(7406):254-8 PMID: 22722828
  28. Water taste: the importance of osmotic sensing in the oral cavity.
    J Water Health. 2006;4 Suppl 1:35-40 PMID: 16493898
  29. Centromere remodeling in Hoolock leuconedys (Hylobatidae) by a new transposable element unique to the gibbons.
    Genome Biol Evol. 2012;4(7):648-58 PMID: 22593550
  30. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data.
    Genome Res. 2010 Sep;20(9):1297-303 PMID: 20644199
  31. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects.
    BMC Bioinformatics. 2011 Dec 22;12:491 PMID: 22192575
  32. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
    Genome Biol. 2014;15(12):550 PMID: 25516281
  33. An exogenous retrovirus isolated from koalas with malignant neoplasias in a US zoo.
    Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11547-52 PMID: 23798387
  34. A transcriptome resource for the koala (Phascolarctos cinereus): insights into koala retrovirus transcription and sequence diversity.
    BMC Genomics. 2014 Sep 11;15:786 PMID: 25214207
  35. Structural features of the rice chromosome 4 centromere.
    Nucleic Acids Res. 2004 Apr 02;32(6):2023-30 PMID: 15064362
  36. Phylogenetic and functional analysis of the vertebrate cytochrome p450 2 family.
    J Mol Evol. 2011 Jan;72(1):56-71 PMID: 21116621
  37. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates.
    Genome Res. 2009 Feb;19(2):327-35 PMID: 19029536
  38. The evolution of marsupial and monotreme chromosomes.
    Cytogenet Genome Res. 2012;137(2-4):113-29 PMID: 22777195
  39. Characterization of the antimicrobial peptide family defensins in the Tasmanian devil (Sarcophilus harrisii), koala (Phascolarctos cinereus), and tammar wallaby (Macropus eugenii).
    Immunogenetics. 2017 Mar;69(3):133-143 PMID: 27838759
  40. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis.
    Gene. 1995 Dec 29;167(1-2):GC1-10 PMID: 8566757
  41. Water as an independent taste modality.
    Front Neurosci. 2010 Oct 15;4:175 PMID: 21048894
  42. Pathogenesis of progressive scarring trachoma in Ethiopia and Tanzania and its implications for disease control: two cohort studies.
    PLoS Negl Trop Dis. 2015 May 13;9(5):e0003763 PMID: 25970613
  43. Tandem repeats finder: a program to analyze DNA sequences.
    Nucleic Acids Res. 1999 Jan 15;27(2):573-80 PMID: 9862982
  44. New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago.
    Science. 2001 Jun 8;292(5523):1888-92 PMID: 11397939
  45. COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients.
    Mol Ecol Resour. 2011 Jan;11(1):141-5 PMID: 21429111
  46. Mammals from 'down under': a multi-gene species-level phylogeny of marsupial mammals (Mammalia, Metatheria).
    PeerJ. 2015 Feb 26;3:e805 PMID: 25755933
  47. Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire.
    Mol Biol Evol. 2014 Feb;31(2):303-9 PMID: 24202612
  48. Predicting the probability of outbreeding depression.
    Conserv Biol. 2011 Jun;25(3):465-75 PMID: 21486369
  49. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences.
    Nature. 2007 May 10;447(7141):167-77 PMID: 17495919
  50. The sequence and de novo assembly of the giant panda genome.
    Nature. 2010 Jan 21;463(7279):311-7 PMID: 20010809
  51. Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas.
    Vet Microbiol. 2013 Aug 30;165(3-4):214-23 PMID: 23523170
  52. Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice.
    Genome Res. 2015 Aug;25(8):1125-34 PMID: 26129709
  53. Reversal and convergence in marsupial chromosome evolution.
    Cytogenet Genome Res. 2003;102(1-4):282-90 PMID: 14970718
  54. The molecular receptive ranges of human TAS2R bitter taste receptors.
    Chem Senses. 2010 Feb;35(2):157-70 PMID: 20022913
  55. Frequency and distribution of cyanogenic glycosides in Eucalyptus L'Hérit.
    Phytochemistry. 2008 Jun;69(9):1870-4 PMID: 18474385
  56. OrthoMCL: identification of ortholog groups for eukaryotic genomes.
    Genome Res. 2003 Sep;13(9):2178-89 PMID: 12952885
  57. Exon capture phylogenomics: efficacy across scales of divergence.
    Mol Ecol Resour. 2016 Sep;16(5):1059-68 PMID: 26215687
  58. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  59. Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development.
    Genome Biol. 2011 Aug 29;12(8):R81 PMID: 21854559
  60. Endogenous Gibbon Ape Leukemia Virus Identified in a Rodent (Melomys burtoni subsp.) from Wallacea (Indonesia).
    J Virol. 2016 Aug 26;90(18):8169-80 PMID: 27384662
  61. A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres.
    Chromosoma. 2009 Feb;118(1):113-25 PMID: 18839199
  62. Retroviral invasion of the koala genome.
    Nature. 2006 Jul 6;442(7098):79-81 PMID: 16823453
  63. Eucalyptus foliar chemistry explains selective feeding by koalas.
    Biol Lett. 2005 Mar 22;1(1):64-7 PMID: 17148129
  64. Immunome database for marsupials and monotremes.
    BMC Immunol. 2011 Aug 19;12:48 PMID: 21854560
  65. In vitro hepatic microsomal metabolism of meloxicam in koalas (Phascolarctos cinereus), brushtail possums (Trichosurus vulpecula), ringtail possums (Pseudocheirus peregrinus), rats (Rattus norvegicus) and dogs (Canis lupus familiaris).
    Comp Biochem Physiol C Toxicol Pharmacol. 2014 Apr;161:7-14 PMID: 24345479
  66. Expression of aquaporin water channels in rat taste buds.
    Chem Senses. 2007 Jun;32(5):411-21 PMID: 17339611
  67. Clinical pharmacokinetics of meloxicam. A cyclo-oxygenase-2 preferential nonsteroidal anti-inflammatory drug.
    Clin Pharmacokinet. 1999 Feb;36(2):115-26 PMID: 10092958
  68. New and emerging chlamydial infections of creatures great and small.
    New Microbes New Infect. 2017 Apr 18;18:28-33 PMID: 28560043
  69. Genome analysis of the platypus reveals unique signatures of evolution.
    Nature. 2008 May 8;453(7192):175-83 PMID: 18464734
  70. Conservation genetics of the koala (Phascolarctos cinereus). II. Limited variability in minisatellite DNA sequences.
    Biochem Genet. 1991 Aug;29(7-8):355-63 PMID: 1747097
  71. Trachoma and Ocular Chlamydial Infection in the Era of Genomics.
    Mediators Inflamm. 2015;2015:791847 PMID: 26424969
  72. Climate change not to blame for late Quaternary megafauna extinctions in Australia.
    Nat Commun. 2016 Jan 29;7:10511 PMID: 26821754
  73. Frequent expansions of the bitter taste receptor gene repertoire during evolution of mammals in the Euarchontoglires clade.
    Mol Biol Evol. 2014 Aug;31(8):2018-31 PMID: 24758778
  74. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement.
    PLoS One. 2014 Nov 19;9(11):e112963 PMID: 25409509
  75. Sequencing of a rice centromere uncovers active genes.
    Nat Genet. 2004 Feb;36(2):138-45 PMID: 14716315
  76. Microsomal metabolism of the terpene 1,8-cineole in the common brushtail possum (Trichosurus vulpecula), koala (Phascolarctos cinereus), rat and human.
    Xenobiotica. 2001 Apr;31(4):205-21 PMID: 11465406
  77. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation.
    Nucleic Acids Res. 2016 Jan 4;44(D1):D733-45 PMID: 26553804
  78. Reconstruction of the ancestral marsupial karyotype from comparative gene maps.
    BMC Evol Biol. 2013 Nov 21;13:258 PMID: 24261750
  79. The genome of Eucalyptus grandis.
    Nature. 2014 Jun 19;510(7505):356-62 PMID: 24919147
  80. BEDTools: a flexible suite of utilities for comparing genomic features.
    Bioinformatics. 2010 Mar 15;26(6):841-2 PMID: 20110278
  81. Conservation genetics of the koala (Phascolarctos cinereus): low mitochondrial DNA variation amongst southern Australian populations.
    Genet Res. 1997 Feb;69(1):25-33 PMID: 9164173
  82. Inference of human population history from individual whole-genome sequences.
    Nature. 2011 Jul 13;475(7357):493-6 PMID: 21753753
  83. Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement.
    Proc Natl Acad Sci U S A. 2015 Apr 14;112(15):4531-40 PMID: 25675493
  84. Koala retrovirus: a genome invasion in real time.
    Genome Biol. 2006;7(11):241 PMID: 17118218
  85. Cloning and expression of koala (Phascolarctos cinereus) liver cytochrome P450 CYP4A15.
    Gene. 2006 Jul 5;376(1):123-32 PMID: 16677781
  86. Genetic drift, selection and the evolution of the mutation rate.
    Nat Rev Genet. 2016 Oct 14;17(11):704-714 PMID: 27739533
  87. BLAST+: architecture and applications.
    BMC Bioinformatics. 2009 Dec 15;10:421 PMID: 20003500
  88. Historically low mitochondrial DNA diversity in koalas (Phascolarctos cinereus).
    BMC Genet. 2012 Oct 24;13:92 PMID: 23095716
  89. A beginner's guide to eukaryotic genome annotation.
    Nat Rev Genet. 2012 Apr 18;13(5):329-42 PMID: 22510764
  90. Human occupation of northern Australia by 65,000 years ago.
    Nature. 2017 Jul 19;547(7663):306-310 PMID: 28726833
  91. Phylogenetic analysis of diprotodontian marsupials based on complete mitochondrial genomes.
    Genes Genet Syst. 2006 Jun;81(3):181-91 PMID: 16905872
  92. Gene finding in novel genomes.
    BMC Bioinformatics. 2004 May 14;5:59 PMID: 15144565
  93. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma.
    Chromosoma. 1985;91(3-4):313-21 PMID: 2579778
  94. Triadic IBD coefficients and applications to estimating pairwise relatedness.
    Genet Res. 2007 Jun;89(3):135-53 PMID: 17894908
Article Info
Journal
Nature genetics
Abbr.
Nat Genet
ISSN
1546-1718
Published
2018-00-00
Epub
2018-00-02
Pages
1102-1111
Language
English
Region
United States
NLM ID
9216904
PMCID
PMC6197426
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/J004669/1 · United Kingdom
NIGMS NIH HHS · R01 GM092706 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]