Volume 42 Issue 5
Sep.  2021
Turn off MathJax
Article Contents
Zhi-Qiang Han, Xin-Yu Guo, Qun Liu, Shan-Shan Liu, Zhi-Xin Zhang, Shi-Jun Xiao, Tian-Xiang Gao. Whole-genome resequencing of Japanese whiting (Sillago japonica) provide insights into local adaptations. Zoological Research, 2021, 42(5): 548-561. doi: 10.24272/j.issn.2095-8137.2021.116
Citation: Zhi-Qiang Han, Xin-Yu Guo, Qun Liu, Shan-Shan Liu, Zhi-Xin Zhang, Shi-Jun Xiao, Tian-Xiang Gao. Whole-genome resequencing of Japanese whiting (Sillago japonica) provide insights into local adaptations. Zoological Research, 2021, 42(5): 548-561. doi: 10.24272/j.issn.2095-8137.2021.116

Whole-genome resequencing of Japanese whiting (Sillago japonica) provide insights into local adaptations

doi: 10.24272/j.issn.2095-8137.2021.116
Funds:  The study was supported by the National Natural Science Foundation of China (41976083, 41776171 and 32072980)
More Information
  • The genetic adaptations of various organisms to heterogeneous environments in the northwestern Pacific remain poorly understood. Heterogeneous genomic divergence among populations may reflect environmental selection. Advancing our understanding of the mechanisms by which organisms adapt to different temperatures in response to climate change and predicting the adaptive potential and ecological consequences of anthropogenic global warming are critical. We sequenced the whole genomes of Japanese whiting (Sillago japonica) specimens collected from different latitudinal locations along the coastal waters of China and Japan to detect possible thermal adaptations. Using population genomics, a total of 5.48 million single nucleotide polymorphisms (SNPs) from five populations revealed a complete genetic break between the Chinese and Japanese groups, which was attributed to both geographic distance and local adaptation. The shared natural selection genes between two isolated populations (i.e., Zhoushan and Ise Bay/Tokyo Bay) indicated possible parallel evolution at the genetic level induced by temperature. These genes also indicated that the process of temperature selection on isolated populations is repeatable. Moreover, we observed natural candidate genes related to membrane fluidity, possibly underlying adaptation to cold environmental stress. These findings advance our understanding of the genetic mechanisms underlying the rapid adaptations of fish species. Species distribution projection models suggested that the Chinese and Japanese groups may have different responses to future climate change, with the former expanding and the latter contracting. The findings of this study enhance our understanding of genetic differentiation and adaptation to changing environments.
  • loading
  • [1]
    Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19(9): 1655−1664. doi: 10.1101/gr.094052.109
    Assis J, Tyberghein L, Bosch S, Verbruggen H, Serrão EA, De Clerck O. 2018. Bio-ORACLE v2.0: Extending marine data layers for bioclimatic modelling. Global Ecology and Biogeography, 27(3): 277−284. doi: 10.1111/geb.12693
    Balanyà J, Huey RB, Gilchrist GW, Serra L. 2009. The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity, 103(5): 364−367. doi: 10.1038/hdy.2009.86
    Bálint M, Domisch S, Engelhardt CHM, Haase P, Lehrian S, Sauer J, et al. 2011. Cryptic biodiversity loss linked to global climate change. Nature Climate Change, 1(6): 313−318. doi: 10.1038/nclimate1191
    Barrett RDH, Rogers SM, Schluter D. 2008. Natural selection on a major armor gene in threespine stickleback. Science, 322(5899): 255−257. doi: 10.1126/science.1159978
    Bradbury IR, Hubert S, Higgins B, Borza T, Bowman S, Paterson IG, et al. 2010. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proceedings of the Royal Society B: Biological Sciences, 277(1701): 3725−3734. doi: 10.1098/rspb.2010.0985
    Cai RS, Han ZQ, Yang ZX. 2020. Impacts and risks of changing ocean on marine ecosystems and dependent communities and related responses. Climate Change Research, 16(2): 182−193. (in Chinese)
    Cardona A, Pagani L, Antao T, Lawson DJ, Eichstaedt CA, Yngvadottir B, et al. 2014. Genome-wide analysis of cold adaptation in indigenous Siberian populations. PLoS One, 9(5): e98076. doi: 10.1371/journal.pone.0098076
    Chen C, Wang HH, Liu ZG, Chen X, Tang J, Meng FM, et al. 2018a. Population genomics provide insights into the evolution and adaptation of the eastern honey bee (Apis cerana). Molecular Biology and Evolution, 35(9): 2260−2271. doi: 10.1093/molbev/msy130
    Chen ZQ, Farrell AP, Matala A, Hoffman N, Narum SR. 2018b. Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates. Evolutionary Applications, 11(9): 1686−1699. doi: 10.1111/eva.12672
    Closs EI, Gräf P, Habermeier A, Cunningham JM, Förstermann U. 1997. Human cationic amino acid transporters hCAT-1, hCAT-2A, and hCAT-2B: three related carriers with distinct transport properties. Biochemistry, 36(21): 6462−6468. doi: 10.1021/bi962829p
    Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. 2011. The variant call format and VCFtools. Bioinformatics, 27(15): 2156−2158. doi: 10.1093/bioinformatics/btr330
    Dong M, Yang XY, Lim S, Cao ZQ, Honek J, Lu HX, et al. 2013. Cold exposure promotes atherosclerotic plaque growth and instability via UCP1-dependent lipolysis. Cell Metabolism, 18(1): 118−129. doi: 10.1016/j.cmet.2013.06.003
    Dray S, Dufour AB. 2007. The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22(4): 1−20.
    Ferchaud AL, Hansen MM. 2016. The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three-spine sticklebacks in divergent environments. Molecular Ecology, 25(1): 238−259. doi: 10.1111/mec.13399
    Fustier MA, Brandenburg JT, Boitard S, Lapeyronnie J, Eguiarte LE, Vigouroux Y, et al. 2017. Signatures of local adaptation in lowland and highland teosintes from whole-genome sequencing of pooled samples. Molecular Ecology, 26(10): 2738−2756. doi: 10.1111/mec.14082
    Gao TX, Wan ZZ, Song N, Zhang XM, Han ZQ. 2014. Evolutionary mechanisms shaping the genetic population structure of coastal fish: insight from populations of Coilia nasus in Northwestern Pacific. Mitochondrial DNA, 25(6): 464−472. doi: 10.3109/19401736.2013.814109
    Gao TX, Yang TY, Yanagimoto T, Xiao YS. 2019. Levels and patterns of genetic variation in Japanese whiting (Sillago japonica) based on mitochondrial DNA control region. Mitochondrial DNA Part A, 30(1): 172−183. doi: 10.1080/24701394.2018.1467411
    Guan BX, Mao HL. 1982. A note on circulation of the East China Sea. Chinese Journal of Oceanology and Limnology, 1(1): 5−16. doi: 10.1007/BF02852887
    Han ZQ, Gao TX, Yanagimoto T, Sakurai Y. 2008. Deep phylogeographic break among white croaker Pennahia argentata (Sciaenidae, Perciformes) populations in North-western Pacific. Fisheries Science, 74(4): 770−780. doi: 10.1111/j.1444-2906.2008.01588.x
    Han ZQ, Han G, Wang ZY, Gao TX. 2015. The possible physical barrier and coastal dispersal strategy for Japanese grenadier anchovy, Coilia nasus in the East China Sea and Yellow Sea: Evidence from AFLP Markers. International Journal of Molecular Sciences, 16(2): 3283−3297. doi: 10.3390/ijms16023283
    Han ZQ, Wang ZY, Gao TX, Yanagimoto T, Iida K. 2018. Assessing the speciation of a cold water species, Japanese sand lance Ammodytes personatus, in the Northwestern Pacific by AFLP Markers. Animals, 8(12): 224. doi: 10.3390/ani8120224
    Hansen PS, Defesche JC, Kastelein JJP, Gerdes LU, Fraza L, Gerdes C, et al. 1997. Phenotypic variation in patients heterozygous for familial defective apolipoprotein B (FDB) in three European countries. Arteriosclerosis, Thrombosis, and Vascular Biology, 17(4): 741−747. doi: 10.1161/01.ATV.17.4.741
    Hu CW, Hu CH, Wu-Chou YH, Lo LJ. 2018. SLC22A5 mutations in a patient with systemicprimary carnitine deficiency and cleft palate-successful perioperative management. Journal of Craniofacial Surgery, 29(6): 1601−1603. doi: 10.1097/SCS.0000000000004595
    Kashiwagi K, Kondo S, Yoshida W, Yoshioka M. 2000. Effects of temperature and salinity on hatching success of Japanese whiting Sillago japonica eggs. Aquaculture Science, 48(4): 637−642.
    Kawahata H, Ohshima H. 2004. Vegetation and environmental record in the northern East China Sea during the late Pleistocene. Global and Planetary Change, 41(3–4): 251−273.
    Kawate H, Itoh R, Sakumi K, Nakabeppu Y, Tsuzuki T, Ide F, et al. 2000. A defect in a single allele of the Mlh1 gene causes dissociation of the killing and tumorigenic actions of an alkylating carcinogen in methyltransferase-deficient mice. Carcinogenesis, 21(2): 301−305. doi: 10.1093/carcin/21.2.301
    Lamichhaney S, Fuentes-Pardo AP, Rafati N, Ryman N, McCracken GR, Bourne C, et al. 2017. Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean. Proceedings of the National Academy of Sciences of the United States of America, 114(17): E3452−E3461. doi: 10.1073/pnas.1617728114
    Leonard WR, Snodgrass JJ, Sorensen MV. 2005. Metabolic adaptation in indigenous Siberian populations. Annual Review of Anthropology, 34: 451−471. doi: 10.1146/annurev.anthro.34.081804.120558
    Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1754−1760. doi: 10.1093/bioinformatics/btp324
    Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature, 475(7357): 493−496. doi: 10.1038/nature10231
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352
    Li YL, Xue DX, Zhang BD, Liu JX. 2019. Population genomic signatures of genetic structure and environmental selection in the catadromous roughskin sculpin Trachidermus fasciatus. Genome Biology and Evolution, 11(7): 1751−1764. doi: 10.1093/gbe/evz118
    Li ZY, Yu L, Zhang YZ, Gao J, Zhang PZ, Wan B, et al. 2001. Identification of human, mouse and rat PPP1R14A, protein phosphatase-1 inhibitor subunit 14A, & mapping human PPP1R14A to chromosome 19q13.13-q13.2. Molecular Biology Reports, 28(2): 91−101. doi: 10.1023/A:1017998029053
    Liu BJ, Zhang BD, Xue DX, Gao TX, Liu JX. 2016. Population structure and adaptive divergence in a high gene flow marine fish: The small yellow croaker (Larimichthys polyactis). PLoS One, 11(4): e0154020. doi: 10.1371/journal.pone.0154020
    Liu LL, Zhu H, Yan YC, Wang XW, Zhang R, Zhu JY. 2018. Research progress of cold tolerance mechanism and functional genes in fish. Biotechnology Bulletin, 34(8): 50−57. (in Chinese)
    Maksimov EG, Mironov KS, Trofimova MS, Nechaeva NL, Todorenko DA, Klementiev KE, et al. 2017. Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria. Photosynthesis Research, 133(1–3): 215−223.
    Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, Yuasa M, et al. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature, 399(6737): 700−704. doi: 10.1038/21447
    McKay RJ. 1992. Sillaginid fishes of the world (Family Sillaginidae). Rome: Food and Agriculture Organization of the United Nations.
    Oka OBV, Pringle MA, Schopp IM, Braakman I, Bulleid NJ. 2013. ERdj5 is the ER reductase that catalyzes the removal of non-native disulfides and correct folding of the LDL receptor. Molecular Cell, 50(6): 793−804. doi: 10.1016/j.molcel.2013.05.014
    Oozeki Y, Hwang PP, Hirano R. 1992. Larval development of the Japanese whiting, Sillago japonica. Japanese Journal of Ichthyology, 39(1): 59−66. doi: 10.1007/BF02905634
    Oshima S, Nakamura T, Namiki S, Okada E, Tsuchiya K, Okamoto R, et al. 2004. Interferon Regulatory Factor 1 (IRF-1) and IRF-2 distinctively up-regulate gene expression and production of interleukin-7 in human intestinal epithelial cells. Molecular and Cellular Biology, 24(14): 6298−6310. doi: 10.1128/MCB.24.14.6298-6310.2004
    Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3–4): 231−259.
    Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8(11): e1002967. doi: 10.1371/journal.pgen.1002967
    Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 81(3): 559−575. doi: 10.1086/519795
    Rouhiainen A, Zhao X, Vanttola P, Qian K, Kulesskiy E, Kuja-Panula J, et al. 2016. HMGB4 is expressed by neuronal cells and affects the expression of genes involved in neural differentiation. Scientific Reports, 6: 32960. doi: 10.1038/srep32960
    Russell NJ, Nichols DS. 1999. Polyunsaturated fatty acids in marine bacteria-a dogma rewritten. Microbiology, 145(4): 767−779. doi: 10.1099/13500872-145-4-767
    Schluter D, McPeek MA. 2000. Ecological character displacement in adaptive radiation. The American Naturalist, 156(S4): S4−S16. doi: 10.1086/303412
    Skelly DK, Joseph LN, Possingham HP, Freidenburg LK, Farrugia TJ, Kinnison MT, et al. 2007. Evolutionary responses to climate change. Conservation Biology, 21(5): 1353−1355. doi: 10.1111/j.1523-1739.2007.00764.x
    Spivakov M, Auer TO, Peravali R, Dunham I, Dolle D, Fujiyama A, et al. 2014. Genomic and phenotypic characterization of a wild medaka population: towards the establishment of an isogenic population genetic resource in fish. G3: Genes-Genomes-Genetics, 4(3): 433−445.
    van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9(2): 112−124. doi: 10.1038/nrm2330
    Wang J, Xue DX, Zhang BD, Li YL, Liu BJ, Liu JX. 2016. Genome-wide SNP discovery, genotyping and their preliminary applications for population genetic inference in spotted sea bass (Lateolabrax maculatus). PLoS One, 11(6): e0157809. doi: 10.1371/journal.pone.0157809
    Wang K, Li MY, Hakonarson H. 2010. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 38(16): e164. doi: 10.1093/nar/gkq603
    White CR, Alton LA, Frappell PB. 2012. Metabolic cold adaptation in fishes occurs at the level of whole animal, mitochondria and enzyme. Proceedings of the Royal Society B: Biological Sciences, 279(1734): 1740−1747. doi: 10.1098/rspb.2011.2060
    Wu X, Huang W, Prasad PD, Seth P, Rajan DP, Leibach FH, et al. 1999. Functional characteristics and tissue distribution pattern of organic cation transporter 2 (OCTN2), an organic cation/carnitine transporter. Journal of Pharmacology and Experimental Therapeutics, 290(3): 1482−1492.
    Xu SY, Song N, Zhao LL, Cai SS, Han ZQ, Gao TX. 2017. Genomic evidence for local adaptation in the ovoviviparous marine fish Sebastiscus marmoratus with a background of population homogeneity. Scientific Reports, 7(1): 1562. doi: 10.1038/s41598-017-01742-z
    Xu SY, Yanagimoto T, Song N, Cai SS, Gao TX, Zhang XM. 2019. Population genomics reveals possible genetic evidence for parallel evolution of Sebastiscus marmoratus in the northwestern Pacific Ocean. Open Biology, 9: 190028. doi: 10.1098/rsob.190028
    Xue TQ, Du N, Gao TX. 2010. Phylogenetic relationships of 4 Sillaginidae species based on partial sequences of COI and cytochrome b gene. Journal of Ocean University China, 40(S1): 91−98. (in Chinese)
    Yamada K, Ono M, Perkins ND, Rocha S, Lamond AI. 2013. Identification and functional characterization of FMN2, a regulator of the cyclin-dependent kinase inhibitor p21. Molecular Cell, 49(5): 922−933. doi: 10.1016/j.molcel.2012.12.023
    Yamamoto T, Davis CG, Brown MS, Schneider WJ, Casey ML, Goldstein JL, et al. 1984. The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell, 39(1): 27−38. doi: 10.1016/0092-8674(84)90188-0
    Yang J, Lee SH, Goddard ME, Visscher PM. 2011. GCTA: a tool for genome-wide complex trait analysis. The American Journal of Human Genetics, 88(1): 76−82. doi: 10.1016/j.ajhg.2010.11.011
    Yang TY, Gao TX, Meng W, Jiang YL. 2020. Genome-wide population structure and genetic diversity of Japanese whiting (Sillago japonica) inferred from genotyping-by-sequencing (GBS): Implications for fisheries management. Fisheries Research, 225: 105501. doi: 10.1016/j.fishres.2020.105501
    Zhang ZX, Xu SY, Capinha C, Weterings R, Gao TX. 2019. Using species distribution model to predict the impact of climate change on the potential distribution of Japanese whiting Sillago japonica. Ecological Indicators, 104: 333−340. doi: 10.1016/j.ecolind.2019.05.023
  • ZR-2021-116 Supplementary Materials.pdf
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(5)  / Tables(2)

    Article Metrics

    Article views (1238) PDF downloads(229) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint