Volume 43 Issue 5
Sep.  2022
Turn off MathJax
Article Contents
Rui-Xiang Tang, Jiao Wang, Yi-Fei Li, Cheng-Ran Zhou, Guan-Liang Meng, Feng-Jun Li, Yue Lan, Megan Price, Lars Podsiadlowski, Yan Yu, Xu-Ming Wang, Yin-Xun Liu, Bi-Song Yue, Shan-Lin Liu, Zhen-Xin Fan, Shao-Ying Liu. Genomics and morphometrics reveal the adaptive evolution of pikas. Zoological Research, 2022, 43(5): 813-826. doi: 10.24272/j.issn.2095-8137.2022.072
Citation: Rui-Xiang Tang, Jiao Wang, Yi-Fei Li, Cheng-Ran Zhou, Guan-Liang Meng, Feng-Jun Li, Yue Lan, Megan Price, Lars Podsiadlowski, Yan Yu, Xu-Ming Wang, Yin-Xun Liu, Bi-Song Yue, Shan-Lin Liu, Zhen-Xin Fan, Shao-Ying Liu. Genomics and morphometrics reveal the adaptive evolution of pikas. Zoological Research, 2022, 43(5): 813-826. doi: 10.24272/j.issn.2095-8137.2022.072

Genomics and morphometrics reveal the adaptive evolution of pikas

doi: 10.24272/j.issn.2095-8137.2022.072
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (31470110, 31970399) and China National GeneBank (CNGB)
More Information
  • Corresponding author: E-mail: zxfan@scu.edu.cnshaoyliu@163.com
  • Received Date: 2022-06-16
  • Accepted Date: 2022-08-18
  • Published Online: 2022-08-22
  • Publish Date: 2022-09-18
  • Pikas (Lagomorpha: Ochotonidae) are small mouse-like lagomorphs. To investigate their adaptation to different ecological environments during their dispersal from the Qinghai-Xizang (Tibet) Plateau (QTP), we collected 226 pikas and measured 20 morphological characteristics and recorded habitat information. We also sequenced the genome of 81 specimens, representing 27 putative pika species. The genome-wide tree based on 4 090 coding genes identified five subgenera, i.e., Alienauroa, Conothoa, Lagotona, Ochotona, and Pika, consistent with morphometric data. Morphologically, Alienauroa and Ochotona had similar traits, including smaller size and earlier divergence time compared to other pikas. Consistently, the habitats of Alienauroa and Ochotona differed from those of the remaining subgenera. Phylogenetic signal analysis detected 83 genes significantly related to morphological characteristics, including several visual and hearing-related genes. Analysis of shared amino acid substitutions and positively selected genes (PSGs) in Alienauroa and Ochotona identified two genes, i.e., mitochondrial function-related TSFM (p.Q155E) and low-light visual sensitivity-related PROM1 (p.H419Y). Functional experiments demonstrated that TSFM-155E significantly enhanced mitochondrial function compared to TSFM-155Q in other pikas, and PROM1-419Y decreased the modeling of dynamic intracellular chloride efflux upon calcium uptake. Alienauroa and Ochotona individuals mostly inhabit different environments (e.g., subtropical forests) than other pikas, suggesting that a shift from the larger ancestral type and changes in sensory acuity and energy enhancement may have been required in their new environments. This study increases our understanding of the evolutionary history of pikas.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403−410. doi: 10.1016/S0022-2836(05)80360-2
    [2]
    Blomberg SP, Garland T Jr, Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57(4): 717−745. doi: 10.1111/j.0014-3820.2003.tb00285.x
    [3]
    Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25(15): 1972−1973. doi: 10.1093/bioinformatics/btp348
    [4]
    Carss KJ, Arno G, Erwood M, Stephens J, Sanchis-Juan A, Hull S, et al. 2017. Comprehensive rare variant analysis via whole-genome sequencing to determine the molecular pathology of inherited retinal disease. The American Journal of Human Genetics, 100(1): 75−90. doi: 10.1016/j.ajhg.2016.12.003
    [5]
    Cehajic-Kapetanovic J, Birtel J, McClements ME, Shanks ME, Clouston P, Downes SM, et al. 2019. Clinical and molecular characterization of PROM1-related retinal degeneration. JAMA Network Open, 2(6): e195752. doi: 10.1001/jamanetworkopen.2019.5752
    [6]
    Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. 2021. Twelve years of SAMtools and BCFtools. GigaScience, 10(2): giab008. doi: 10.1093/gigascience/giab008
    [7]
    Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. 2020. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37(1): 291−294. doi: 10.1093/molbev/msz189
    [8]
    Dellett M, Sasai N, Nishide K, Becker S, Papadaki V, Limb GA, et al. 2015. Genetic background and light-dependent progression of photoreceptor cell degeneration in Prominin-1 knockout mice. Investigative Ophthalmology & Visual Science, 56(1): 164−176.
    [9]
    Di Nottia M, Montanari A, Verrigni D, Oliva R, Torraco A, Fernandez-Vizarra E, et al. 2017. Novel mutation in mitochondrial Elongation Factor EF-Tu associated to dysplastic leukoencephalopathy and defective mitochondrial DNA translation. Biochimica et Biophysica Acta-Molecular Basis of Disease, 1863(4): 961−967. doi: 10.1016/j.bbadis.2017.01.022
    [10]
    Feng ZJ, Zheng CL. 1985. Studies on the pikas (genus: Ochotona) of China—Taxonomic notes and distribution. Acta Theriologica Sinica, 5(4): 269−289. (in Chinese)
    [11]
    Fujinami K, Oishi A, Yang LZ, Arno G, Pontikos N, Yoshitake K, et al. 2020. Clinical and genetic characteristics of 10 Japanese patients with PROM1-associated retinal disorder: a report of the phenotype spectrum and a literature review in the Japanese population. American Journal of Medical Genetics Part C:Seminars in Medical Genetics, 184(3): 656−674. doi: 10.1002/ajmg.c.31826
    [12]
    Ge DY, Wen ZX, Xia L, Zhang ZQ, Erbajeva M, Huang CM, et al. 2013. Evolutionary history of lagomorphs in response to global environmental change. PLos One, 8(4): e59668. doi: 10.1371/journal.pone.0059668
    [13]
    Ge DY, Zhang ZQ, Xia L, Zhang Q, Ma Y, Yang QS. 2012. Did the expansion of C4 plants drive extinction and massive range contraction of micromammals? Inferences from food preference and historical biogeography of pikas. Palaeogeography, Palaeoclimatology, Palaeoecology, 326–328: 160–171.
    [14]
    Gong ZD, Wang YX, Li ZH, Li SQ. 2000. A new species of pika: pianma blacked pika, Ochotona nigritia (Lagomorpha: Ochotonidae) from Yunnan, China. Zoological Research, 21(3): 204−209. (in Chinese)
    [15]
    Gonzalez-Freire M, de Cabo R, Bernier M, Sollott SJ, Fabbri E, Navas P, et al. 2015. Reconsidering the role of mitochondria in aging. The Journals of Gerontology:Series A, 70(11): 1334−1342. doi: 10.1093/gerona/glv070
    [16]
    Grevendonk L, Connell NJ, McCrum C, Fealy CE, Bilet L, Bruls YMH, et al. 2021. Impact of aging and exercise on skeletal muscle mitochondrial capacity, energy metabolism, and physical function. Nature Communications, 12(1): 4773. doi: 10.1038/s41467-021-24956-2
    [17]
    Gu ZG, Eils R, Schlesner M. 2016. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics, 32(18): 2847−2849. doi: 10.1093/bioinformatics/btw313
    [18]
    Hargreaves M, Spriet LL. 2018. Exercise metabolism: fuels for the fire. Cold Spring Harbor Perspectives in Medicine, 8(8): a029744. doi: 10.1101/cshperspect.a029744
    [19]
    Henry P, Russello MA. 2013. Adaptive divergence along environmental gradients in a climate-change-sensitive mammal. Ecology and Evolution, 3(11): 3906−3917. doi: 10.1002/ece3.776
    [20]
    Hori A, Nishide K, Yasukuni Y, Haga K, Kakuta W, Ishikawa Y, et al. 2019. Prominin-1 modulates Rho/ROCK-mediated membrane morphology and calcium-dependent intracellular chloride flux. Scientific Reports, 9(1): 15911. doi: 10.1038/s41598-019-52040-9
    [21]
    Huang J, Liang XM, Xuan YK, Geng CY, Li YX, Lu HR, et al. 2017. A reference human genome dataset of the BGISEQ-500 sequencer. GigaScience, 6(5): gix024.
    [22]
    Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, et al. 2002. The Ensembl genome database project. Nucleic Acids Research, 30(1): 38−41. doi: 10.1093/nar/30.1.38
    [23]
    Institute of Vertebrate Paleontology CaOS. 1960. Handbook of Vertebrate Fossils of China - Part of Mammals. Beijing: Science Press, 232. (in Chinese)
    [24]
    Jespersgaard C, Fang MY, Bertelsen M, Dang X, Jensen H, Chen YL, et al. 2019. Molecular genetic analysis using targeted NGS analysis of 677 individuals with retinal dystrophy. Scientific Reports, 9(1): 1219. doi: 10.1038/s41598-018-38007-2
    [25]
    Jin M, Li S, Moghrabi WN, Sun H, Travis GH. 2005. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell, 122(3): 449−459.
    [26]
    Jo DH, Song DW, Cho CS, Kim UG, Lee KJ, Lee K, et al. 2019. CRISPR-Cas9-mediated therapeutic editing of Rpe65 ameliorates the disease phenotypes in a mouse model of Leber congenital amaurosis. Science Advances, 5(10): eaax1210. doi: 10.1126/sciadv.aax1210
    [27]
    Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4): 772−780. doi: 10.1093/molbev/mst010
    [28]
    Koju NP, He K, Chalise MK, Ray C, Chen ZZ, Zhang B, et al. 2017. Multilocus approaches reveal underestimated species diversity and inter-specific gene flow in pikas (Ochotona) from southwestern China. Molecular Phylogenetics and Evolution, 107: 239−245. doi: 10.1016/j.ympev.2016.11.005
    [29]
    Konarzewski M, Książek A. 2013. Determinants of intra-specific variation in basal metabolic rate. Journal of Comparative Physiology B, 183(1): 27−41. doi: 10.1007/s00360-012-0698-z
    [30]
    Kozlov AM, Aberer AJ, Stamatakis A. 2015. ExaML version 3: a tool for phylogenomic analyses on supercomputers. Bioinformatics, 31(15): 2577−2579. doi: 10.1093/bioinformatics/btv184
    [31]
    Kristensen TN, Ketola T, Kronholm I. 2020. Adaptation to environmental stress at different timescales. Annals of the New York Academy of Sciences, 1476(1): 5−22. doi: 10.1111/nyas.13974
    [32]
    Kumaran N, Ali RR, Tyler NA, Bainbridge JWB, Michaelides M, Rubin GS. 2020. Validation of a vision-guided mobility assessment for RPE65-associated retinal dystrophy. Translational Vision Science & Technology, 9(10): 5.
    [33]
    Lanier HC, Olson LE. 2009. Inferring divergence times within pikas (Ochotona spp. ) using mtDNA and relaxed molecular dating techniques. Molecular Phylogenetics and Evolution, 53(1): 1−12. doi: 10.1016/j.ympev.2009.05.035
    [34]
    Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv: 1303.3997.
    [35]
    Lissovsky AA. 2013. Taxonomic revision of pikas Ochotona (Lagomorpha, Mammalia) at the species level. Mammalia, 78(2): 199−216.
    [36]
    Lissovsky AA, Yatsentyuk SP, Koju NP. 2019. Multilocus phylogeny and taxonomy of pikas of the subgenus Ochotona (Lagomorpha, Ochotonidae). Zoologica Scripta, 48(1): 1−16. doi: 10.1111/zsc.12325
    [37]
    Liu SY, Jin W, Liao R, Sun ZY, Zeng T, Fu JR, et al. 2017. Phylogenetic study of Ochotona based on mitochondrial Cyt b and morphology with a description of one new subgenus and five new species. Acta Theriologica Sinica, 37(1): 1−43. (in Chinese) doi: 10.1016/j.chnaes.2016.09.003
    [38]
    Löytynoja A. 2014. Phylogeny-aware alignment with PRANK. In: Russell DJ. Multiple Sequence Alignment Methods. Totowa: Humana Press, 155–170.
    [39]
    Maino JL, Kearney MR. 2014. Ontogenetic and interspecific metabolic scaling in insects. The American Naturalist, 184(6): 695−701. doi: 10.1086/678401
    [40]
    Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, Bridges RJ, et al. 2000. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Human Molecular Genetics, 9(1): 27−34. doi: 10.1093/hmg/9.1.27
    [41]
    Melo-Ferreira J, de Matos AL, Areal H, Lissovsky AA, Carneiro M, Esteves PJ. 2015. The phylogeny of pikas (Ochotona) inferred from a multilocus coalescent approach. Molecular Phylogenetics and Evolution, 84: 240−244. doi: 10.1016/j.ympev.2015.01.004
    [42]
    Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, et al. 2011. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science, 334(6055): 521−524. doi: 10.1126/science.1211028
    [43]
    Michaelides M, Gaillard MC, Escher P, Tiab L, Bedell M, Borruat FX, et al. 2010. The PROM1 mutation p. R373C causes an autosomal dominant bull's eye maculopathy associated with rod, rod-cone, and macular dystrophy. Investigative Ophthalmology & Visual Science, 51(9): 4771−4780.
    [44]
    Moses ME, Hou C, Woodruff WH, West GB, Nekola JC, Zuo WY, et al. 2008. Revisiting a model of ontogenetic growth: estimating model parameters from theory and data. The American Naturalist, 171(5): 632−645. doi: 10.1086/587073
    [45]
    Motta FL, Martin RP, Porto FBO, Wohler ES, Resende RG, Gomes CP, et al. 2020. Pathogenicity reclasssification of RPE65 missense variants related to leber congenital amaurosis and early-onset retinal dystrophy. Genes, 11(1): 24.
    [46]
    Niu Yd, Wei FW, Li M, Liu Xm, Feng ZJ. 2004. Phylogeny of pikas (Lagomorpha, Ochotona) inferred from mitochondrial cytochrome b sequences. Folia Zoologica -Praha, 53(2): 141−155.
    [47]
    Null R, Team R, Null R, Writing TC, Null R, Team R, et al. 2011. R: a language and environment for statistical computing. 1: 12–21.
    [48]
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Wagner H. 2019. Vegan: community ecology package, v. 2.5--6.
    [49]
    Otto EA, Loeys B, Khanna H, Hellemans J, Sudbrak R, Fan SL, et al. 2005. Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nature Genetics, 37(3): 282−288. doi: 10.1038/ng1520
    [50]
    Pan Y, Kelly LE, El-Hodiri HM. 2018. Identification of retinal homeobox (rax) gene-dependent genes by a microarray approach: the DNA endoglycosylase neil3 is a major downstream component of the rax genetic pathway. Developmental Dynamics, 247(11): 1199−1210. doi: 10.1002/dvdy.24679
    [51]
    Paradis E, Schliep K. 2019. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3): 526−528. doi: 10.1093/bioinformatics/bty633
    [52]
    Parsons PA. 2005. Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biological Reviews, 80(4): 589−610. doi: 10.1017/S1464793105006822
    [53]
    Rankin AM, Galbreath KE, Teeter KC. 2017. Signatures of adaptive molecular evolution in American pikas (Ochotona princeps). Journal of Mammalogy, 98(4): 1156−1167. doi: 10.1093/jmammal/gyx059
    [54]
    Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, et al. 2019. g: Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Research, 47(W1): W191−W198. doi: 10.1093/nar/gkz369
    [55]
    Revell LJ. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2): 217−223. doi: 10.1111/j.2041-210X.2011.00169.x
    [56]
    Revelle W. 2020. psych: Procedures for Personality and Psychological Research, v=2.0. 12. Evanston, Illinois, USA: Northwestern University,https://CRAN.R-project.org/package=psych.
    [57]
    Sato M, Nakazawa M, Usui T, Tanimoto N, Abe H, Ohguro H. 2005. Mutations in the gene coding for guanylate cyclase-activating protein 2 (GUCA1B gene) in patients with autosomal dominant retinal dystrophies. Graefe's Archive for Clinical and Experimental Ophthalmology, 243(3): 235−242. doi: 10.1007/s00417-004-1015-7
    [58]
    Scala M, Brigati G, Fiorillo C, Nesti C, Rubegni A, Pedemonte M, et al. 2019. Novel homozygous TSFM pathogenic variant associated with encephalocardiomyopathy with sensorineural hearing loss and peculiar neuroradiologic findings. Neurogenetics, 20(3): 165−172. doi: 10.1007/s10048-019-00582-5
    [59]
    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11): 2498−2504. doi: 10.1101/gr.1239303
    [60]
    Sikes RS, Gannon WL. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92(1): 235−253. doi: 10.1644/10-MAMM-F-355.1
    [61]
    Silva RS, Salles MV, Motta FL, Sallum JMF. 2020. Retinitis pigmentosa due to Rp1 biallelic variants. Scientific Reports, 10(1): 1603. doi: 10.1038/s41598-020-58243-9
    [62]
    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31(19): 3210−3212. doi: 10.1093/bioinformatics/btv351
    [63]
    Smeitink JAM, Elpeleg O, Antonicka H, Diepstra H, Saada A, Smits P, et al. 2006. Distinct clinical phenotypes associated with a mutation in the mitochondrial translation elongation factor EFTs. The American Journal of Human Genetics, 79(5): 869−877. doi: 10.1086/508434
    [64]
    Smith AT, Johnston CH, Alves PC, Hackländer K. 2018. Lagomorphs: Pikas, Rabbits, and Hares of the World. Baltimore: Johns Hopkins University Press.
    [65]
    Smith AT, Smith HJ, Wang XG, Yin XC, Liang J. 1986. Social behavior of the steppe-dwelling black-lipped pika (ochotona curzoniae). Acta Theriologica Sinica, 6(1): 13−32.
    [66]
    Smith AT, Xie Y. 2009. A guide to the Mammals of China. Changsha: Hunan Education Press. (in Chinese)
    [67]
    Sokolov VE, Ivanitskaya EY, Gruzdev VV, Heptner VG. 2009. Lagomorphs: Mammals of Russia and Adjacent Regions. Boca Raton: CRC Press.
    [68]
    Song J, Smaoui N, Ayyagari R, Stiles D, Benhamed S, MacDonald IM, et al. 2011. High-throughput retina-array for screening 93 genes involved in inherited retinal dystrophy. Investigative Ophthalmology & Visual Science, 52(12): 9053−9060.
    [69]
    Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9): 1312−1313. doi: 10.1093/bioinformatics/btu033
    [70]
    Sukhotin A, Kovalev A, Sokolov E, Sokolova IM. 2020. Mitochondrial performance of a continually growing marine bivalve, Mytilus edulis, depends on body size. Journal of Experimental Biology, 223(13): jeb226332.
    [71]
    Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34(S2): W609−W612.
    [72]
    Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. 2017. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Research, 45(D1): D362−D368. doi: 10.1093/nar/gkw937
    [73]
    Wang XY, Liang D, Jin W, Tang MK, Shalayiwu, Liu SY, et al. 2020. Out of Tibet: genomic perspectives on the evolutionary history of extant pikas. Molecular Biology and Evolution, 37(6): 1577−1592. doi: 10.1093/molbev/msaa026
    [74]
    Wang Y. 1988. Ochotona gaoligongensis-a new species. Zoological Research: 9 (in Chinese)
    [75]
    Wang YX. 2003. Taxonomic list and distribution of mammal species and subspecies in China. Beijing: China Forestry Publishing House (in Chinese)
    [76]
    Wieden HJ, Gromadski K, Rodnin D, Rodnina MV. 2002. Mechanism of elongation factor (EF)-Ts-catalyzed nucleotide exchange in EF-Tu - Contribution of contacts at the guanine base. Journal of Biological Chemistry, 277(8): 6032−6036. doi: 10.1074/jbc.M110888200
    [77]
    Wilson DE, Reeder DM. 1993. Mammal Species of the World: A Taxonomic and Geographic Reference. 2nd ed. Washington: Smithsonian Press.
    [78]
    Wilson DE, Reeder DM. 2005. Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd ed. Baltimore: Johns Hopkins University Press.
    [79]
    Wilson MC, Smith AT. 2015. The pika and the watershed: the impact of small mammal poisoning on the ecohydrology of the Qinghai-Tibetan Plateau. Ambio, 44(1): 16−22. doi: 10.1007/s13280-014-0568-x
    [80]
    Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8): 1586−1591. doi: 10.1093/molbev/msm088
    [81]
    Yu L, Wang GD, Ruan J, Chen YB, Yang CP, Cao X, et al. 2016. Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation. Nature Genetics, 48(8): 947−952. doi: 10.1038/ng.3615
    [82]
    Yu Y, Blair C, He XJ. 2020. RASP 4: ancestral state reconstruction tool for multiple genes and characters. Molecular Biology and Evolution, 37(2): 604−606. doi: 10.1093/molbev/msz257
    [83]
    Zachos J, Pagani M, Sloan L, Thomas E, Billups K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292(5517): 686−693. doi: 10.1126/science.1059412
    [84]
    Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics, 19(S6): 153. doi: 10.1186/s12859-018-2129-y
    [85]
    Zhang HF. 2021. DNA short-insert library construction protocol for illumina HiSeq 2500/4000/X ten or NovaSeq.
    [86]
    Zhang QJ, Zulfiqar F, Xiao XS, Riazuddin SA, Ahmad Z, Caruso R, et al. 2007. Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Human Genetics, 122(3–4): 293–299.
  • ZR-2022-072 Supplementary Materials.rar
  • 加载中

Catalog

    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(4)

    Article Metrics

    Article views (870) PDF downloads(160) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return