Cited by 45Genomics and Phylogenetic StudiesChromosomal and Genetic VariationsMarine animal studies overview

The first chromosome‐level genome for a marine mammal as a resource to study ecology and evolution

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Fan, Guangyi, Zhang, Yaolei, Liu, Xiaochuan, Wang, Jiahao, Sun, Zeguo, Sun, Shuai, Zhang, He, Chen, Jianwei +38 more·2019·Molecular Ecology Resources

Abstract

Marine mammals are important models for studying convergent evolution and aquatic adaption, and thus reference genomes of marine mammals can provide evolutionary insights. Here, we present the first chromosome‐level marine mammal genome assembly based on the data generated by the BGISEQ‐500 platform, for a stranded female sperm whale (Physeter macrocephalus). Using this reference genome, we performed chromosome evolution analysis of the sperm whale, including constructing ancestral chromosomes, identifying chromosome rearrangement events and comparing with cattle chromosomes, which provides a resource for exploring marine mammal adaptation and speciation. We detected a high proportion of long interspersed nuclear elements and expanded gene families, and contraction of major histocompatibility complex region genes which were specific to sperm whale. Using comparisons with sheep and cattle, we analysed positively selected genes to identify gene pathways that may be related to adaptation to the marine environment. Further, we identified possible convergent evolution in aquatic mammals by testing for positively selected genes across three orders of marine mammals. In addition, we used publicly available resequencing data to confirm a rapid decline in global population size in the Pliocene to Pleistocene transition. This study sheds light on the chromosome evolution and genetic mechanisms underpinning sperm whale adaptations, providing valuable resources for future comparative genomics.

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  • Comparing a highly-fragmented with a highly-contiguous assembly of two sperm whale species showed that orthologous genes located on a single scaffold in both species have a much higher sequence identity (mean 98.70%) than paralogous genes (mean 75.18%).

    “Indeed, comparing a highly-fragmented with a highly-contiguous assembly of two sperm whale species (27, 29) showed that orthologous genes located on a single scaffold in both species have a much higher sequence identity (mean 98.70%) than paralogous genes (mean 75.18%) (Fig. 4B).”

    From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [29]

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Research works printed but not linked: 72

  1. Aedo, J. E., Maldonado, J., Aballai, V., Estrada, J. M., Bastias-Molina, M., Meneses, C., . . . Valdés, J. A. (2015). mRNA-seq reveals skeletal muscle atrophy in response to handling stress in a marine teleost, the red cusk-eel (Genypterus chilensis). BMC genomics, 16(1), 1024.
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol, 215(3), 403-410. doi:10.1016/S0022- 2836(05)80360-2 · DOI · Paper page
  3. Arnason, U. (1974). Comparative chromosome studies in Cetacea. Hereditas, 77(1), 1-36.
  4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., . . . Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet, 25(1), 25-29. doi:10.1038/75556 · DOI · Paper page
  5. Bairoch, A., & Apweiler, R. (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res, 28(1), 45-48.
  6. Bao, W., Kojima, K. K., & Kohany, O. (2015). Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA, 6, 11. doi:10.1186/s13100-015-0041-9 · DOI
  7. Birney, E., Clamp, M., & Durbin, R. (2004). GeneWise and Genomewise. Genome Res, 14(5), 988-995. doi:10.1101/gr.1865504 · DOI
  8. Bru, C., Courcelle, E., Carrere, S., Beausse, Y., Dalmar, S., & Kahn, D. (2005). The ProDom database of protein domain families: more emphasis on 3D. Nucleic Acids Res, 33(Database issue), D212-215. doi:10.1093/nar/gki034 · DOI
  9. Burge, C., & Karlin, S. (1997). Prediction of complete gene structures in human genomic DNA. J Mol Biol, 268(1), 78-94. doi:10.1006/jmbi.1997.0951 · DOI
  10. Burwinkel, B., & Kilimann, M. W. (1998). Unequal homologous recombination between LINE-1 elements as a mutational mechanism in human genetic disease. J Mol Biol, 277(3), 513-517. doi:10.1006/jmbi.1998.1641 · DOI
  11. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 540-552.
  12. Chang, C. C., Chow, C. C., Tellier, L. C., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015). Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience, 4, 7. doi:10.1186/s13742-015-0047-8 · DOI · Paper page
  13. Dudchenko, O., Batra, S. S., Omer, A. D., Nyquist, S. K., Hoeger, M., Durand, N. C., . . . Aiden, E. L. (2017). De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science, 356(6333), 92-95. doi:10.1126/science. · DOI · Paper page
  14. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research, 32(5), 1792-1797.
  15. Eichler, E. E., & Sankoff, D. (2003). Structural dynamics of eukaryotic chromosome evolution. Science, 301(5634), 793-797.
  16. Elsik, C. G., Mackey, A. J., Reese, J. T., Milshina, N. V., Roos, D. S., & Weinstock, G. M. (2007). Creating a honey bee consensus gene set. Genome biology, 8(1), 1.
  17. Fan, G., Chen, J., Jin, T., Shi, C., Du, X., Zhang, H., . . . Liu , X. L. (2018). The Report of Marine Life Genomic Research. Preprints. doi:10.20944/preprints201812.0156.v1 · DOI
  18. Ferguson-Smith, M. A., & Trifonov, V. (2007). Mammalian karyotype evolution. Nature Reviews Genetics, 8(12), 950.
  19. Foote, A. D., Liu, Y., Thomas, G. W., Vinař, T., Alföldi, J., Deng, J., . . . Joshi, V. (2015). Convergent evolution of the genomes of marine mammals. Nature genetics, 47(3), 272.
  20. Fuchs, G., Hollander, D., Voichek, Y., Ast, G., & Oren, M. (2014). Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate. Genome research, 24(10), 1572-1583.
  21. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., . . . Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol, 29(7), 644-652. doi:10.1038/nbt.1883 · DOI
  22. Hahn, M. W., De Bie, T., Stajich, J. E., Nguyen, C., & Cristianini, N. (2005). Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome research, 15(8), 1153-1160.
  23. Hulo, N., Bairoch, A., Bulliard, V., Cerutti, L., De Castro, E., Langendijk-Genevaux, P. S., . . . Sigrist, C. J. (2006). The PROSITE database. Nucleic Acids Res, 34(Database issue), D227-230. doi:10.1093/nar/gkj063 · DOI
  24. Jackson, J. A., Baker, C. S., Vant, M., Steel, D. J., Medrano-Gonzalez, L., & Palumbi, S. R. (2009). Big and slow: phylogenetic estimates of molecular evolution in baleen whales (suborder mysticeti). Mol Biol Evol, 26(11), 2427-2440. doi:10.1093/molbev/msp169 · DOI
  25. Jaillon, O., Aury, J.-M., Brunet, F., Petit, J.-L., Stange-Thomann, N., Mauceli, E., . . . Bernot, A. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature, 431(7011), 946.
  26. Kalujnaia, S., McVee, J., Kasciukovic, T., Stewart, A. J., & Cramb, G. (2010). A role for inositol monophosphatase 1 (IMPA1) in salinity adaptation in the euryhaline eel (Anguilla anguilla). FASEB J, 24(10), 3981-3991. doi:10.1096/fj.10-161000 · DOI
  27. Kanehisa, M., & Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res, 28(1), 27-30.
  28. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780.
  29. Kellis, M., Birren, B. W., & Lander, E. S. (2004). Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature, 428(6983), 617.
  30. Kirkpatrick, M. (2010). How and why chromosome inversions evolve. PLoS biology, 8(9), e1000501.
  31. Kooyman, G., & Ponganis, P. (1998). The physiological basis of diving to depth: birds and mammals. Annual Review of Physiology, 60(1), 19-32.
  32. Kosugi, S., Hirakawa, H., & Tabata, S. (2015). GMcloser: closing gaps in assemblies accurately with a likelihood-based selection of contig or long-read alignments. Bioinformatics, 31(23), 3733-3741.
  33. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., . . . Marra, M. A. (2009). Circos: an information aesthetic for comparative genomics. Genome Res, 19(9), 1639-1645. doi:10.1101/gr.092759.109 · DOI
  34. Li, H., Coghlan, A., Ruan, J., Coin, L. J., Heriche, J. K., Osmotherly, L., . . . Durbin, R. (2006). TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res, 34(Database issue), D572-580. doi:10.1093/nar/gkj118 · DOI · Paper page
  35. Li, H., & Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26(5), 589-595. doi:10.1093/bioinformatics/btp698 · DOI · Paper page
  36. Li, H., & Durbin, R. (2011). Inference of human population history from individual whole- genome sequences. Nature, 475(7357), 493-496. doi:10.1038/nature10231 · DOI · Paper page
  37. Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., . . . Liu, Y. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience, 1(1), 18.
  38. Mak, S. S. T., Gopalakrishnan, S., Caroe, C., Geng, C., Liu, S., Sinding, M. S., . . . Gilbert, M. T. P. (2017). Comparative performance of the BGISEQ-500 vs Illumina HiSeq2500 sequencing platforms for palaeogenomic sequencing. Gigascience, 6(8), 1-13. doi:10.1093/gigascience/gix049 · DOI
  39. Marino, L. (2004). Cetacean brain evolution: multiplication generates complexity. International Journal of Comparative Psychology, 17(1).
  40. Mi, H., Lazareva-Ulitsky, B., Loo, R., Kejariwal, A., Vandergriff, J., Rabkin, S., . . . Thomas, P. D. (2005). The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res, 33(Database issue), D284-288. doi:10.1093/nar/gki078 · DOI
  41. Nakatani, Y., Takeda, H., Kohara, Y., & Morishita, S. (2007). Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res, 17(9), 1254-1265. doi:10.1101/gr.6316407 · DOI · Paper page
  42. Perrin, W. F., Würsig, B., & Thewissen, J. (2009). Encyclopedia of marine mammals: Academic Press.
  43. Pertea, M., Kim, D., Pertea, G. M., Leek, J. T., & Salzberg, S. L. (2016). Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc, 11(9), 1650-1667. doi:10.1038/nprot.2016.095 · DOI
  44. Ponting, C. P., Schultz, J., Milpetz, F., & Bork, P. (1999). SMART: identification and annotation of domains from signalling and extracellular protein sequences. Nucleic Acids Res, 27(1), 229-232.
  45. Price, M. N., Dehal, P. S., & Arkin, A. P. (2010). FastTree 2-approximately maximum- likelihood trees for large alignments. PloS one, 5(3), e9490.
  46. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., . . . Finn, R. D. (2012). The Pfam protein families database. Nucleic Acids Res, 40(Database issue), D290-301. doi:10.1093/nar/gkr1065 · DOI · Paper page
  47. Repanas, K., Zingler, N., Layer, L. E., Schumann, G. G., Perrakis, A., & Weichenrieder, O. (2007). Determinants for DNA target structure selectivity of the human LINE-1 retrotransposon endonuclease. Nucleic acids research, 35(14), 4914-4926.
  48. Rockman, M. V., Skrovanek, S. S., & Kruglyak, L. (2010). Selection at linked sites shapes heritable phenotypic variation in C. elegans. Science, 330(6002), 372-376.
  49. Salse, J., Bolot, S., Throude, M., Jouffe, V., Piegu, B., Quraishi, U. M., . . . Feuillet, C. (2008). Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. The Plant Cell, 20(1), 11-24.
  50. Schreer, J. F., & Kovacs, K. M. (1997). Allometry of diving capacity in air-breathing vertebrates. Canadian Journal of Zoology, 75(3), 339-358.
  51. Segal, Y., Peissel, B., Renieri, A., de Marchi, M., Ballabio, A., Pei, Y., & Zhou, J. (1999). LINE-1 elements at the sites of molecular rearrangements in Alport syndrome-diffuse leiomyomatosis. Am J Hum Genet, 64(1), 62-69. doi:10.1086/302213 · DOI
  52. Sharma, R., Kishore, A., Mukesh, M., Ahlawat, S., Maitra, A., Pandey, A. K., & Tantia, M. S. (2015). Genetic diversity and relationship of Indian cattle inferred from microsatellite and mitochondrial DNA markers. BMC Genet, 16, 73. doi:10.1186/s12863-015-0221- 0 · DOI
  53. Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31(19), 3210-3212.
  54. Smith, T. D., Reeves, R. R., Josephson, E. A., & Lund, J. N. (2012). Spatial and seasonal distribution of American whaling and whales in the age of sail. PloS one, 7(4), e34905.
  55. Spehr, M., Kelliher, K. R., Li, X.-H., Boehm, T., Leinders-Zufall, T., & Zufall, F. (2006). Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. Journal of Neuroscience, 26(7), 1961- 1970.
  56. Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S., & Morgenstern, B. (2006). AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res, 34(Web Server issue), W435-439. doi:10.1093/nar/gkl200 · DOI · Paper page
  57. Takeshima, S. N., & Aida, Y. (2006). Structure, function and disease susceptibility of the bovine major histocompatibility complex. Animal Science Journal, 77(2), 138-150.
  58. Tarailo-Graovac, M., & Chen, N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics, Chapter 4, Unit 4 10. doi:10.1002/0471250953. · DOI
  59. Tyack, P. L., Johnson, M., Soto, N. A., Sturlese, A., & Madsen, P. T. (2006). Extreme diving of beaked whales. Journal of Experimental Biology, 209(21), 4238-4253.
  60. UniProt, C. (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res, 40(Database issue), D71-75. doi:10.1093/nar/gkr981 · DOI
  61. Van der Auwera, G. A., Carneiro, M. O., Hartl, C., Poplin, R., Del Angel, G., Levy- Moonshine, A., . . . DePristo, M. A. (2013). From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics, 43, 11 10 11-33. doi:10.1002/0471250953. · DOI
  62. Warren, W. C., Kuderna, L., Alexander, A., Catchen, J., Perez-Silva, J. G., Lopez-Otin, C., . . . Wise, J. P., Sr. (2017). The Novel Evolution of the Sperm Whale Genome. Genome Biol Evol, 9(12), 3260-3264. doi:10.1093/gbe/evx187 · DOI
  63. Watwood, S. L., Miller, P. J., Johnson, M., Madsen, P. T., & Tyack, P. L. (2006). Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus). J Anim Ecol, 75(3), 814-825. doi:10.1111/j.1365-2656.2006.01101.x · DOI
  64. Weichenrieder, O., Repanas, K., & Perrakis, A. (2004). Crystal structure of the targeting endonuclease of the human LINE-1 retrotransposon. Structure, 12(6), 975-986.
  65. Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M., & Jaffe, D. B. (2017). Direct determination of diploid genome sequences. Genome Res, 27(5), 757-767. doi:10.1101/gr.214874.116 · DOI · Paper page
  66. Wienberg, J. (2004). The evolution of eutherian chromosomes. Curr Opin Genet Dev, 14(6), 657-666. doi:10.1016/j.gde.2004.10.001 · DOI
  67. Xu, Z., & Wang, H. (2007). LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res, 35(Web Server issue), W265-268. doi:10.1093/nar/gkm286 · DOI
  68. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8), 1586-1591.
  69. Yim, H.-S., Cho, Y. S., Guang, X., Kang, S. G., Jeong, J.-Y., Cha, S.-S., . . . Kwon, K. K. (2014). Minke whale genome and aquatic adaptation in cetaceans. Nature genetics, 46(1), 88.
  70. Younger, R. M., Amadou, C., Bethel, G., Ehlers, A., Lindahl, K. F., Forbes, S., . . . Trowsdale, J. (2001). Characterization of clustered MHC-linked olfactory receptor genes in human and mouse. Genome research, 11(4), 519-530.
  71. Zdobnov, E. M., & Apweiler, R. (2001). InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics, 17(9), 847-848.
  72. Zhou, X., Guang, X., Sun, D., Xu, S., Li, M., Seim, I., . . . Yang, G. (2018). Population genomics of finless porpoises reveal an incipient cetacean species adapted to freshwater. Nat Commun, 9(1), 1276. doi:10.1038/s41467-018-03722-x · DOI

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Authors
Fan, G., Zhang, Y., Liu, X., Wang, J., Sun, Z., Sun, S., Zhang, H., Chen, J., Lv, M., Han, K., Tan, X., Hu, J., Guan, R., Fu, Y., Liu, S., Chen, X., Xu, Q., Qin, Y., Liu, L., Bai, J., Wang, O., Tang, J., Lu, H., Shang, Z., Wang, B., Hu, G., Zhao, X., Zou, Y., Chen, A., Gong, M., Zhang, W., Lee, S. M. ‐., Li, S., Liu, J., Li, Z., Lu, Y., Sabir, J. S. M., Sabir, M. J., Khan, M., Hajrah, N. H., Yin, Y., Kristiansen, K., Yang, H., Wang, J., Xu, X., & Liu, X.
Affiliations
  • BGI Group (China) (CN)
  • Guangdong Pearl River Estuary Chinese White Dolphin National Nature Reserve Administration Zhu Hai Guangdong China
  • China National GeneBank (CN)
  • University of Macau (MO)
  • Chinese Academy of Sciences (CN)
  • Health and Family Planning Integrated Supervision Enforcement Bureau of Shinan District Qingdao City China
  • Guangdong Ocean University (CN)
  • King Abdulaziz University (SA)
  • University of Copenhagen (DK)
Corresponding author
Liu, Xin
Venue
Molecular Ecology Resources
Publisher
Wiley
Published
2019-05-09
Volume
19
Issue
4
Pages
944-956
ISSN
  • 1755-098X (ISSN-L)
  • 1755-0998
OpenAlex
W2914147444
Cited by
45
References
3
Citations by year
2026: 6 · 2025: 4 · 2024: 7 · 2023: 7 · 2022: 5 · 2021: 4 · 2020: 6 · 2019: 5
FWCI
1.72
Type
journal article
Language
en
Open access
Locations
  • Molecular Ecology Resources (publishedVersion)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
  • Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, other-oa)
Funders
Government of Jiangxi Province
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Physical Sciences › Environmental Science › Ecology › Marine animal studies overview
Keywords
sperm whale, chromosome-level genome assembly, karyotype evolution, ancestral chromosomes, chromosomal rearrangements, convergent evolution, aquatic adaptation, long interspersed nuclear elements, major histocompatibility complex, positive selection, population decline, Pliocene-Pleistocene transition, comparative genomics
MeSH terms
Adaptation, Biological, Animals, Cattle, Female, Sheep, Genome, Ecosystem, Evolution, Molecular, Sperm Whale, Aquatic Organisms

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