Baiji genomes reveal low genetic variability and new insights into secondary aquatic adaptations

The baiji, or Yangtze River dolphin (Lipotes vexillifer), is a flagship species for the conservation of aquatic animals and ecosystems in the Yangtze River of China; however, this species has now been recognized as functionally extinct. Here we report a high-quality draft genome and three re-sequenced genomes of L. vexillifer using Illumina short-read sequencing technology. Comparative genomic analyses reveal that cetaceans have a slow molecular clock and molecular adaptations to their aquatic lifestyle. We also find a significantly lower number of heterozygous single nucleotide polymorphisms in the baiji compared to all other mammalian genomes reported thus far. A reconstruction of the demographic history of the baiji indicates that a bottleneck occurred near the end of the last deglaciation, a time coinciding with a rapid decrease in temperature and the rise of eustatic sea level.

[1]  A. Rambaut,et al.  Determinants of rate variation in mammalian DNA sequence evolution , 1996, Journal of Molecular Evolution.

[2]  J. R. Brandon,et al.  First human-caused extinction of a cetacean species? , 2007, Biology Letters.

[3]  Maria Jesus Martin,et al.  The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 , 2003, Nucleic Acids Res..

[4]  Rolf Apweiler,et al.  The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000 , 2000, Nucleic Acids Res..

[5]  R. Murphy,et al.  Parallel Evolution of Auditory Genes for Echolocation in Bats and Toothed Whales , 2012, PLoS genetics.

[6]  Rolf Apweiler,et al.  The SWISS-PROT protein sequence data bank and its supplement TrEMBL , 1997, Nucleic Acids Res..

[7]  中尾 光輝,et al.  KEGG(Kyoto Encyclopedia of Genes and Genomes)〔和文〕 (特集 ゲノム医学の現在と未来--基礎と臨床) -- (データベース) , 2000 .

[8]  R. Durbin,et al.  Inference of human population history from individual whole-genome sequences. , 2011, Nature.

[9]  D. H. Levenson,et al.  Genetic evidence for the ancestral loss of short-wavelength-sensitive cone pigments in mysticete and odontocete cetaceans , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  R. Britten,et al.  Rates of DNA sequence evolution differ between taxonomic groups. , 1986, Science.

[11]  Huanming Yang,et al.  SNP detection for massively parallel whole-genome resequencing. , 2009, Genome research.

[12]  R. Nielsen,et al.  Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. , 2005, Molecular biology and evolution.

[13]  Steven Salzberg,et al.  TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders , 2004, Bioinform..

[14]  Loretta Auvil,et al.  The yak genome and adaptation to life at high altitude , 2012, Nature Genetics.

[15]  E. Teeling,et al.  Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence , 2011, Heredity.

[16]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

[17]  Huanming Yang,et al.  Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation , 2012, Nature Genetics.

[18]  Bernd Würsig,et al.  Encyclopedia of Marine Mammals , 2001 .

[19]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[20]  Yang Liu,et al.  Convergent sequence evolution between echolocating bats and dolphins , 2010, Current Biology.

[21]  L. Sloan,et al.  Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present , 2001, Science.

[22]  R. Agarwala,et al.  Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST , 2006, BMC Biology.

[23]  J. Reidenberg Anatomical adaptations of aquatic mammals , 2007, Anatomical record.

[24]  R. Durbin,et al.  GeneWise and Genomewise. , 2004, Genome research.

[25]  Ziheng Yang,et al.  Phylogenetic Analysis by Maximum Likelihood (PAML) , 2002 .

[26]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[27]  J. Thewissen,et al.  Evolutionary changes of the importance of olfaction in cetaceans based on the olfactory marker protein gene. , 2012, Gene.

[28]  R. Nielsen,et al.  Patterns of Positive Selection in Six Mammalian Genomes , 2008, PLoS genetics.

[29]  P. Mckinnon DNA repair deficiency and neurological disease , 2009, Nature Reviews Neuroscience.

[30]  M. Springer,et al.  Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins , 2013, PLoS genetics.

[31]  Ramón Doallo,et al.  CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics , 2012, Nature Methods.

[32]  M. Kimura The Neutral Theory of Molecular Evolution: Introduction , 1983 .

[33]  Ya-ping Zhang,et al.  Genome-Wide Scans for Candidate Genes Involved in the Aquatic Adaptation of Dolphins , 2012, Genome biology and evolution.

[34]  Sudhir Kumar,et al.  Mutation rates in mammalian genomes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Alan Hodgkinson,et al.  Variation in the mutation rate across mammalian genomes , 2011, Nature Reviews Genetics.

[36]  M. Bruford,et al.  Conservation Options for the Baiji: Time for Realism? , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[37]  L. Peshkin,et al.  Genome sequencing reveals insights into physiology and longevity of the naked mole rat , 2011, Nature.

[38]  G. Weinstock,et al.  Creating a honey bee consensus gene set , 2007, Genome Biology.

[39]  Stefano Mariani,et al.  Ecological adaptation determines functional mammalian olfactory subgenomes. , 2010, Genome research.

[40]  Dawei Li,et al.  The Genomes of Oryza sativa: A History of Duplications , 2005, PLoS biology.

[41]  K. Holsinger The neutral theory of molecular evolution , 2004 .

[42]  D. Wildman,et al.  Dolphin genome provides evidence for adaptive evolution of nervous system genes and a molecular rate slowdown , 2012, Proceedings of the Royal Society B: Biological Sciences.

[43]  Andrew Rambaut,et al.  Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phylogenies , 2000, Bioinform..

[44]  S. Palumbi,et al.  Big and slow: phylogenetic estimates of molecular evolution in baleen whales (suborder mysticeti). , 2009, Molecular biology and evolution.

[45]  J. Brand,et al.  Major taste loss in carnivorous mammals , 2012, Proceedings of the National Academy of Sciences.

[46]  Sudhir Kumar,et al.  Molecular clocks: four decades of evolution , 2005, Nature Reviews Genetics.

[47]  P. Jeggo,et al.  The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders. , 2008, DNA repair.

[48]  Xuming Zhou,et al.  Phylogenomic analyses and improved resolution of Cetartiodactyla. , 2011, Molecular phylogenetics and evolution.

[49]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[50]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[51]  John Gatesy,et al.  The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods. , 2008, Systematic biology.

[52]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[53]  Andrew P. Martin,et al.  Body size, metabolic rate, generation time, and the molecular clock. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[54]  K. Miller,et al.  The Phanerozoic Record of Global Sea-Level Change , 2005, Science.

[55]  S. Rossiter,et al.  Cetaceans on a Molecular Fast Track to Ultrasonic Hearing , 2010, Current Biology.

[56]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[57]  Huanming Yang,et al.  De novo assembly of human genomes with massively parallel short read sequencing. , 2010, Genome research.

[58]  Joan O. Grimalt,et al.  Molecular biomarker record of sea surface temperature and climatic change in the South China Sea during the last 140,000 years , 1999 .

[59]  Reproductive Biology and Phylogeny of Cetacea : Whales, Porpoises and Dolphins , 2007 .

[60]  P. Hof,et al.  Phylogenomic analyses reveal convergent patterns of adaptive evolution in elephant and human ancestries , 2009, Proceedings of the National Academy of Sciences.