Evolutionary and biomedical insights from a marmoset diploid genome assembly.

Animals Biomedical Research Callithrix / genetics DNA Copy Number Variations Diploidy Evolution, Molecular Female Genome / genetics Genomics / standards Germ-Line Mutation / genetics Haplotypes / genetics Heterozygote Humans INDEL Mutation / genetics Male Reference Standards Selection, Genetic Sex Differentiation / genetics Y Chromosome / genetics

Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
06 2021
Historique:
received: 20 09 2020
accepted: 12 04 2021
pubmed: 29 4 2021
medline: 3 8 2021
entrez: 28 4 2021
Statut: ppublish

Résumé

The accurate and complete assembly of both haplotype sequences of a diploid organism is essential to understanding the role of variation in genome functions, phenotypes and diseases

Identifiants

DOI: 10.1038/s41586-021-03535-x PMID: 33910227 PMC: PMC8189906
pubmed: 33910227
doi: 10.1038/s41586-021-03535-x
pii: 10.1038/s41586-021-03535-x
pmc: PMC8189906
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

227-233

Subventions

Organisme : NIMH NIH HHS
ID : F30 MH112351
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007739
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States

Références

Aleman, F. The necessity of diploid genome sequencing to unravel the genetic component of complex phenotypes. Front. Genet. 8, 148 (2017).
pubmed: 29075286 pmcid: 5641544 doi: 10.3389/fgene.2017.00148
Okano, H., Hikishima, K., Iriki, A. & Sasaki, E. The common marmoset as a novel animal model system for biomedical and neuroscience research applications. Semin. Fetal Neonatal Med. 17, 336–340 (2012).
pubmed: 22871417 doi: 10.1016/j.siny.2012.07.002
Kishi, N., Sato, K., Sasaki, E. & Okano, H. Common marmoset as a new model animal for neuroscience research and genome editing technology. Dev. Growth Differ. 56, 53–62 (2014).
pubmed: 24387631 doi: 10.1111/dgd.12109
Wood, A. R. et al. Allelic heterogeneity and more detailed analyses of known loci explain additional phenotypic variation and reveal complex patterns of association. Hum. Mol. Genet. 20, 4082–4092 (2011).
pubmed: 21798870 pmcid: 3177649 doi: 10.1093/hmg/ddr328
Chin, C.-S. et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050–1054 (2016).
pubmed: 27749838 pmcid: 5503144 doi: 10.1038/nmeth.4035
Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M. & Jaffe, D. B. Direct determination of diploid genome sequences. Genome Res. 27, 757–767 (2017).
pubmed: 28381613 pmcid: 5411770 doi: 10.1101/gr.214874.116
Koren, S. et al. De novo assembly of haplotype-resolved genomes with trio binning. Nat. Biotechnol. 36, 1174–1182 (2018).
doi: 10.1038/nbt.4277
Rhie, A. et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature https://doi.org/10.1038/s41586-021-03451-0 (2021).
Sherlock, J. K., Griffin, D. K., Delhanty, J. D. A. & Parrington, J. M. Homologies between human and marmoset (Callithrix jacchus) chromosomes revealed by comparative chromosome painting. Genomics 33, 214–219 (1996).
pubmed: 8660970 doi: 10.1006/geno.1996.0186
Benirschke, K., Anderson, J. M. & Brownhill, L. E. Marrow chimerism in marmosets. Science 138, 513–515 (1962).
pubmed: 17753948 doi: 10.1126/science.138.3539.513
Sweeney, C., Ward, J. & Vallender, E. J. Naturally occurring, physiologically normal, primate chimeras. Chimerism 3, 43–44 (2012).
pubmed: 22627807 pmcid: 3442812 doi: 10.4161/chim.20729
The Marmoset Genome Sequencing and Analysis Consortium. The common marmoset genome provides insight into primate biology and evolution. Nat. Genet. 46, 850–857 (2014).
pmcid: 4138798 doi: 10.1038/ng.3042
Sato, K. et al. Resequencing of the common marmoset genome improves genome assemblies and gene-coding sequence analysis. Sci. Rep. 5, 16894 (2015).
pubmed: 26586576 pmcid: 4653617 doi: 10.1038/srep16894
Nembaware, V., Wolfe, K. H., Bettoni, F., Kelso, J. & Seoighe, C. Allele-specific transcript isoforms in human. FEBS Lett. 577, 233–238 (2004).
pubmed: 15527791 doi: 10.1016/j.febslet.2004.10.018
Anton, E., Blanco, J. & Vidal, F. Meiotic behavior of three D;G Robertsonian translocations: segregation and interchromosomal effect. J. Hum. Genet. 55, 541–545 (2010).
pubmed: 20555339 doi: 10.1038/jhg.2010.67
Stankiewicz, P. & Lupski, J. R. Genome architecture, rearrangements and genomic disorders. Trends Genet. 18, 74–82 (2002).
pubmed: 11818139 doi: 10.1016/S0168-9525(02)02592-1
Acuna-Hidalgo, R., Veltman, J. A. & Hoischen, A. New insights into the generation and role of de novo mutations in health and disease. Genome Biol. 17, 241 (2016).
pubmed: 27894357 pmcid: 5125044 doi: 10.1186/s13059-016-1110-1
Goldmann, J. M. et al. Parent-of-origin-specific signatures of de novo mutations. Nat. Genet. 48, 935–939 (2016).
doi: 10.1038/ng.3597 pubmed: 27322544
Chintalapati, M. & Moorjani, P. Evolution of the mutation rate across primates. Curr. Opin. Genet. Dev. 62, 58–64 (2020).
pubmed: 32634682 doi: 10.1016/j.gde.2020.05.028
Zoonomia Consortium. A comparative genomics multitool for scientific discovery and conservation. Nature 587, 240–245 (2020).
doi: 10.1038/s41586-020-2876-6
Vollger, M. R. et al. Long-read sequence and assembly of segmental duplications. Nat. Methods 16, 88–94 (2019).
pubmed: 30559433 doi: 10.1038/s41592-018-0236-3
Bellott, D. W. et al. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508, 494–499 (2014).
pubmed: 24759411 pmcid: 4139287 doi: 10.1038/nature13206
Pfeifer, S. P. Direct estimate of the spontaneous germ line mutation rate in African green monkeys. Evolution 71, 2858–2870 (2017).
pubmed: 29068052 doi: 10.1111/evo.13383
Thomas, G. W. C. et al. Reproductive longevity predicts mutation rates in primates. Curr. Biol. 28, 3193–3197 (2018).
pubmed: 30270182 pmcid: 6177314 doi: 10.1016/j.cub.2018.08.050
Raudsepp, T. & Chowdhary, B. P. The eutherian pseudoautosomal region. Cytogenet. Genome Res. 147, 81–94 (2015).
pubmed: 26730606 doi: 10.1159/000443157
Hinch, A. G., Altemose, N., Noor, N., Donnelly, P. & Myers, S. R. Recombination in the human pseudoautosomal region PAR1. PLoS Genet. 10, e1004503 (2014).
pubmed: 25033397 pmcid: 4102438 doi: 10.1371/journal.pgen.1004503
Holmquist, G. P. Chromosome bands, their chromatin flavors, and their functional features. Am. J. Hum. Genet. 51, 17–37 (1992).
pubmed: 1609794 pmcid: 1682890
Hughes, J. F. & Page, D. C. The biology and evolution of mammalian Y chromosomes. Annu. Rev. Genet. 49, 507–527 (2015).
pubmed: 26442847 doi: 10.1146/annurev-genet-112414-055311
Mueller, J. L. et al. Independent specialization of the human and mouse X chromosomes for the male germ line. Nat. Genet. 45, 1083–1087 (2013).
pubmed: 23872635 pmcid: 3758364 doi: 10.1038/ng.2705
Lucotte, E. A. et al. Dynamic copy number evolution of X- and Y-linked ampliconic genes in human populations. Genetics 209, 907–920 (2018).
pubmed: 29769284 pmcid: 6028258 doi: 10.1534/genetics.118.300826
Bachtrog, D. A dynamic view of sex chromosome evolution. Curr. Opin. Genet. Dev. 16, 578–585 (2006).
pubmed: 17055249 doi: 10.1016/j.gde.2006.10.007
Wahab, F., Drummer, C. & Behr, R. Marmosets. Curr. Biol. 25, R780–R782 (2015).
pubmed: 26394094 doi: 10.1016/j.cub.2015.06.042
Millar, M. R., Sharpe, R. M., Weinbauer, G. F., Fraser, H. M. & Saunders, P. T. Marmoset spermatogenesis: organizational similarities to the human. Int. J. Androl. 23, 266–277 (2000).
pubmed: 11012784 doi: 10.1046/j.1365-2605.2000.00236.x
Cortez, D. et al. Origins and functional evolution of Y chromosomes across mammals. Nature 508, 488–493 (2014).
pubmed: 24759410 doi: 10.1038/nature13151
Havugimana, P. C. et al. A census of human soluble protein complexes. Cell 150, 1068–1081 (2012).
pubmed: 22939629 pmcid: 3477804 doi: 10.1016/j.cell.2012.08.011
Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999).
pubmed: 10542153 doi: 10.1126/science.286.5441.964
Abbott, D. H., Barnett, D. K., Colman, R. J., Yamamoto, M. E. & Schultz-Darken, N. J. Aspects of common marmoset basic biology and life history important for biomedical research. Comp. Med. 53, 339–350 (2003).
pubmed: 14524409
Harris, R. A. et al. Evolutionary genetics and implications of small size and twinning in callitrichine primates. Proc. Natl Acad. Sci. USA 111, 1467–1472 (2014).
pubmed: 24379383 doi: 10.1073/pnas.1316037111
Power, M. L. in The Evolution of Exudativory in Primates 25–44 (Springer, 2010).
Colman, R. J. Absence of estrogen depletion bone loss in female common marmosets. J. Bone Miner. Res. 12, S342 (1997)
Binkley, N. et al. Zoledronate prevents the development of absolute osteopenia following ovariectomy in adult rhesus monkeys. J. Bone Miner. Res. 13, 1775–1782 (1998).
pubmed: 9797488 doi: 10.1359/jbmr.1998.13.11.1775
Saleem, A. N. et al. Mice with alopecia, osteoporosis, and systemic amyloidosis due to mutation in Zdhhc13, a gene coding for palmitoyl acyltransferase. PLoS Genet. 6, e1000985 (2010).
pubmed: 20548961 pmcid: 2883605 doi: 10.1371/journal.pgen.1000985
Iseki, S., Wilkie, A. O. & Morriss-Kay, G. M. Fgfr1 and Fgfr2 have distinct differentiation- and proliferation-related roles in the developing mouse skull vault. Development 126, 5611–5620 (1999).
pubmed: 10572038 doi: 10.1242/dev.126.24.5611
White, K. E. et al. Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am. J. Hum. Genet. 76, 361–367 (2005).
pubmed: 15625620 doi: 10.1086/427956
Moore, H. D. M., Gems, S. & Hearn, J. P. Early implantation stages in the marmoset monkey (Callithrix jacchus). Am. J. Anat. 172, 265–278 (1985).
pubmed: 3922211 doi: 10.1002/aja.1001720402
Saltzman, W., Schultz-Darken, N. J., Severin, J. M. & Abbott, D. H. Escape from social suppression of sexual behavior and of ovulation in female common marmosets. Ann. NY Acad. Sci. 807, 567–570 (1997).
pubmed: 9071400 doi: 10.1111/j.1749-6632.1997.tb51970.x
Mujoomdar, M. L., Hogan, L. M., Parlow, A. F. & Nachtigal, M. W. Pcsk6 mutant mice exhibit progressive loss of ovarian function, altered gene expression, and formation of ovarian pathology. Reproduction 141, 343–355 (2011).
pubmed: 21183657 doi: 10.1530/REP-10-0451
Cho, H. et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485, 123–127 (2012).
pubmed: 22460952 pmcid: 3367514 doi: 10.1038/nature11048
Chomez, P. et al. Increased cell death and delayed development in the cerebellum of mice lacking the rev-erbA(alpha) orphan receptor. Development 127, 1489–1498 (2000).
pubmed: 10704394 doi: 10.1242/dev.127.7.1489
Zhang, Z. et al. TGIF1 and SF1 polymorphisms are associated with litter size in Small Tail Han sheep. Reprod. Domest. Anim. 55, 1145–1153 (2020).
pubmed: 32594576 pmcid: 7540012 doi: 10.1111/rda.13753
Lagasse, E. & Weissman, I. L. Enforced expression of Bcl-2 in monocytes rescues macrophages and partially reverses osteopetrosis in op/op mice. Cell 89, 1021–1031 (1997).
pubmed: 9215625 doi: 10.1016/S0092-8674(00)80290-1
Son, A. et al. Homer2 and Homer3 modulate RANKL-induced NFATc1 signaling in osteoclastogenesis and bone metabolism. J. Endocrinol. 242, 241–249 (2019).
pubmed: 31319381 doi: 10.1530/JOE-19-0123
Tillgren, V., Ho, J. C. S., Önnerfjord, P. & Kalamajski, S. The novel small leucine-rich protein chondroadherin-like (CHADL) is expressed in cartilage and modulates chondrocyte differentiation. J. Biol. Chem. 290, 918–925 (2015).
pubmed: 25451920 doi: 10.1074/jbc.M114.593541
Ludlage, E. & Mansfield, K. Clinical care and diseases of the common marmoset (Callithrix jacchus). Comp. Med. 53, 369–382 (2003).
pubmed: 14524413
Bailey, M. T. & Coe, C. L. Intestinal microbial patterns of the common marmoset and rhesus macaque. Comp. Biochem. Physiol. A. 133, 379–388 (2002).
doi: 10.1016/S1095-6433(02)00174-5
Malukiewicz, J. et al. The gut microbiome of exudivorous wild and captive marmosets. Preprint at https://doi.org/10.1101/708255 (2020).
Turroni, F. et al. Glycan utilization and cross-feeding activities by Bifidobacteria. Trends Microbiol. 26, 339–350 (2018).
pubmed: 29089173 doi: 10.1016/j.tim.2017.10.001
Wiśniewski, J. R., Friedrich, A., Keller, T., Mann, M. & Koepsell, H. The impact of high-fat diet on metabolism and immune defense in small intestine mucosa. J. Proteome Res. 14, 353–365 (2015).
pubmed: 25285821 doi: 10.1021/pr500833v
Plaza-Díaz, J. et al. Adamdec1, Ednrb and Ptgs1/Cox1, inflammation genes upregulated in the intestinal mucosa of obese rats, are downregulated by three probiotic strains. Sci. Rep. 7, 1939 (2017).
pubmed: 28512356 pmcid: 5434015 doi: 10.1038/s41598-017-02203-3
Jordan, D. M. et al. Identification of cis-suppression of human disease mutations by comparative genomics. Nature 524, 225–229 (2015).
pubmed: 26123021 pmcid: 4537371 doi: 10.1038/nature14497
Storz, J. F. Compensatory mutations and epistasis for protein function. Curr. Opin. Struct. Biol. 50, 18–25 (2018).
pubmed: 29100081 doi: 10.1016/j.sbi.2017.10.009
Formenti, G. et al. Complete vertebrate mitogenomes reveal widespread gene duplications and repeats. Preprint at https://doi.org/10.1101/2020.06.30.177956 (2020).
Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020).
pubmed: 31971576 pmcid: 7203741 doi: 10.1093/bioinformatics/btaa025
Lam, E. T. et al. Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat. Biotechnol. 30, 771–776 (2012).
pubmed: 22797562 doi: 10.1038/nbt.2303
Ghurye, J. et al. Integrating Hi-C links with assembly graphs for chromosome-scale assembly. PLOS Comput. Biol. 15, e1007273 (2019).
pubmed: 31433799 pmcid: 6719893 doi: 10.1371/journal.pcbi.1007273
Bishara, A. et al. Read clouds uncover variation in complex regions of the human genome. Genome Res. 25, 1570–1580 (2015).
pubmed: 26286554 pmcid: 4579342 doi: 10.1101/gr.191189.115
Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at https://arxiv.org/abs/1207.3907 (2012).
Chow, W. et al. gEVAL - a web-based browser for evaluating genome assemblies. Bioinformatics 32, 2508–2510 (2016).
pubmed: 27153597 pmcid: 4978925 doi: 10.1093/bioinformatics/btw159
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
Servant, N. et al. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 16, 259 (2015).
pubmed: 26619908 pmcid: 4665391 doi: 10.1186/s13059-015-0831-x
Chakraborty, M., Emerson, J. J., Macdonald, S. J. & Long, A. D. Structural variants exhibit widespread allelic heterogeneity and shape variation in complex traits. Nat. Commun. 10, 4872 (2019).
pubmed: 31653862 pmcid: 6814777 doi: 10.1038/s41467-019-12884-1
Nattestad, M. & Schatz, M. C. Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics 32, 3021–3023 (2016).
pubmed: 27318204 pmcid: 6191160 doi: 10.1093/bioinformatics/btw369
Goel, M., Sun, H., Jiao, W. B. & Schneeberger, K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 20, 277 (2019).
pubmed: 31842948 pmcid: 6913012 doi: 10.1186/s13059-019-1911-0
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).
doi: 10.1038/nbt.1754 pubmed: 21221095 pmcid: 3346182
Löytynoja, A. Phylogeny-aware alignment with PRANK. Methods Mol. Biol. 1079, 155–170 (2014).
pubmed: 24170401 doi: 10.1007/978-1-62703-646-7_10
Sela, I., Ashkenazy, H., Katoh, K. & Pupko, T. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 43), W7–W14 (2015).
pubmed: 25883146 pmcid: 4489236 doi: 10.1093/nar/gkv318
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
pubmed: 17483113 doi: 10.1093/molbev/msm088
Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).
pubmed: 19151095 pmcid: 2672624 doi: 10.1093/bioinformatics/btp033

Auteurs

Chentao Yang (C)

BGI-Shenzhen, Shenzhen, China.
Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Yang Zhou (Y)

BGI-Shenzhen, Shenzhen, China.
ORCID: 0000-0003-1247-5049

Stephanie Marcus (S)

Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA.

Giulio Formenti (G)

Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA.
Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.
ORCID: 0000-0002-7554-5991

Lucie A Bergeron (LA)

Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Zhenzhen Song (Z)

University of the Chinese Academy of Sciences, Beijing, China.

Xupeng Bi (X)

BGI-Shenzhen, Shenzhen, China.

Juraj Bergman (J)

Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark.
ORCID: 0000-0002-9415-2747

Marjolaine Marie C Rousselle (MMC)

Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark.

Chengran Zhou (C)

BGI-Shenzhen, Shenzhen, China.
ORCID: 0000-0002-9468-5973

Long Zhou (L)

BGI-Shenzhen, Shenzhen, China.

Yuan Deng (Y)

BGI-Shenzhen, Shenzhen, China.
Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Miaoquan Fang (M)

BGI-Shenzhen, Shenzhen, China.

Duo Xie (D)

BGI-Shenzhen, Shenzhen, China.
ORCID: 0000-0001-7010-3601

Yuanzhen Zhu (Y)

BGI-Shenzhen, Shenzhen, China.

Shangjin Tan (S)

BGI-Shenzhen, Shenzhen, China.

Jacquelyn Mountcastle (J)

Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.
ORCID: 0000-0003-1078-4905

Bettina Haase (B)

Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.

Jennifer Balacco (J)

Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.

Jonathan Wood (J)

Wellcome Sanger Institute, Hinxton, UK.

William Chow (W)

Wellcome Sanger Institute, Hinxton, UK.

Arang Rhie (A)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
ORCID: 0000-0002-9809-8127

Martin Pippel (M)

Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Center for Systems Biology, Dresden, Germany.
ORCID: 0000-0002-8134-5929

Margaret M Fabiszak (MM)

Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA.
ORCID: 0000-0002-2170-2170

Sergey Koren (S)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
ORCID: 0000-0002-1472-8962

Olivier Fedrigo (O)

Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.
ORCID: 0000-0002-6450-7551

Winrich A Freiwald (WA)

Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA.
Center for Brains, Minds and Machines (CBMM), The Rockefeller University, New York, NY, USA.
ORCID: 0000-0001-8456-5030

Kerstin Howe (K)

Wellcome Sanger Institute, Hinxton, UK.
ORCID: 0000-0003-2237-513X

Huanming Yang (H)

BGI-Shenzhen, Shenzhen, China.
University of the Chinese Academy of Sciences, Beijing, China.
James D. Watson Institute of Genome Sciences, Hangzhou, China.
Guangdong Provincial Academician Workstation of BGI Synthetic Genomics, BGI-Shenzhen, Shenzhen, China.

Adam M Phillippy (AM)

Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
ORCID: 0000-0003-2983-8934

Mikkel Heide Schierup (MH)

Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark.
ORCID: 0000-0002-5028-1790

Erich D Jarvis (ED)

Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA.
Vertebrate Genome Laboratory, The Rockefeller University, New York, NY, USA.
Howard Hughes Medical Institute, Chevy Chase, MD, USA.
ORCID: 0000-0001-8931-5049

Guojie Zhang (G)

Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark. guojie.zhang@bio.ku.dk.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China. guojie.zhang@bio.ku.dk.
China National GeneBank, BGI-Shenzhen, Shenzhen, China. guojie.zhang@bio.ku.dk.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China. guojie.zhang@bio.ku.dk.
ORCID: 0000-0001-6860-1521

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questionsmedicales.fr › Eucaryotes › Animaux › Evolutionary and biomedical insights from a...
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