Abstract
The complex environments and climatic conditions of the Qinghai-Tibet Plateau (QTP) create unique patterns of species diversity. However, the effect of uplift of the QTP on the distribution of Gymnocypris species (Gymnocypris) remain unclear. We found that the Qilian Mountain (QL) population has the highest genetic diversity by mitochondrial DNA hypervariable region of Gymnocypris species, the Tibetan (T) population has the lowest genetic diversity. The T population differs significantly from the Qinghai Lake (QH) and QL populations based on single nucleotide polymorphisms. A phylogeny and network distribution of this species on the QTP reveal differences in its genetic structure and support its taxonomic status. Neutrality tests reveal that Gymnocypris species has experienced different degrees of expansion, even secondary expansion. A divergence timetree estimates that the time of separation of different populations is possible related to uplift of the QTP and is consistent with the time of corresponding geological events. The QL population was separated from the other populations during the third uplift of the QTP (approximately 0.14 million years ago), and the QH and T populations were separated in the late Pleistocene to the Holocene (approximately 0.03 million years ago). In conclusion, this study provides different insights into the distribution of Gymnocypris species due to uplift of the QTP. Gymnocypris species was separated into different populations by this uplift, and each population exhibits unique characteristics, especially in terms of genetic structure and the degree of expansion. Moreover, the divergence time is consistent with the time of uplift of the QTP.
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Data availability
Sequences of mtDNA D-loop of 104 individuals of Gymnocypris species were submitted to GenBank (Accession numbers KJ610703-KJ610806).
References
An Z, Kutzbach J, Prell W (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411:62–66
Bian Q, Liu J, Luo X (2000) Geotectonic setting, formation and evolution of the Qinghai Lake. Dizhen Dizhi 22:20–26
Blanton R, Page L, Hilber S (2013) Timing of clade divergence and discordant estimates of genetic and morphological diversity in the Slender Madtom, Noturus exilis (Ictaluridae). Mol Phylogenet Evol 66:679–693. https://doi.org/10.1016/j.ympev.2012.10.022
Cai Y, Jiao T, Lei Z, Liu L, Zhao S (2018) Maternal genetic and phylogenetic characteristics of domesticated cattle in northwestern China. PLoS ONE 13(12):e0209645. https://doi.org/10.1371/journal.pone.0209645
Cao Y, Chen X, Wang S, Wang Y, Du J (2008) Evolution and regulation of the downstream gene of hypoxia-inducible factor-1alpha in naked carp (Gymnocypris przewalskii) from Lake Qinghai, China. J Mol Evol 67:570–580. https://doi.org/10.1007/s00239-008-9175-4
Che J, Zhou W, Hu J, Yan F, Papenfuss T, Wake D, Zhang Y (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci USA 107:13765–13770. https://doi.org/10.1073/pnas.1008415107
Chen W, Shen Y, Gan X, Wang X, He S (2016) Genetic diversity and evolutionary history of the Schizothorax species complex in the Lancang River (upper Mekong). Ecol Evol 6:6023–6036. https://doi.org/10.1002/ece3.2319
Chi W, Ma X, Niu J, Zou M (2017) Genome-wide identification of genes probably relevant to the adaptation of schizothoracins (Teleostei: Cypriniformes) to the uplift of the Qinghai-Tibet Plateau. BMC Genom. 18:310. https://doi.org/10.1186/s12864-017-3703-9
Christopher N, Balakrishaan S, Minfort A, Lalji S, Michael D (2003) Phyogeography and conservation genetics of Eld’s deer (Cervuseldi). Mol Ecol 12:1–10
Duan Z, Zhao K, Peng Z, Li J, Diogo R, Zhao X, He S (2009) Comparative phylogeography of the Yellow River schizothoracine fishes (Cyprinidae): vicariance, expansion, and recent coalescence in response to the Quaternary environmental upheaval in the Tibetan Plateau. Mol Phylogenet Evol 53:1025–1031
Favre A, Packert M, Pauls S, Jahnig S, Uhl D, Michalak I, Muellner A (2015) The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol Rev Camb Philos Soc 90:236–253. https://doi.org/10.1111/brv.12107
Fu XY (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925. https://doi.org/10.0000/PMID9335623
Guan L, Chi W, Xiao W, Chen L, He S (2014) Analysis of hypoxia-inducible factor alpha polyploidization reveals adaptation to Tibetan plateau in the evolution of schizothoracine fish. BMC Evol Biol 14(1):192
Harrison T, Copeland P, Kidd W, Yin A (1992) Raising tibet. Science 255:1663–1670
He D, Chen Y (2006) Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. J Biogeogr 33:1448–1460. https://doi.org/10.1111/j.1365-2699.2006.01510.x
He D, Chen Y, Liu C, Tao J, Ding C, Chen Y (2016) Comparative phylogeography and evolutionary history of schizothoracine fishes in the Changtang Plateau and their implications for the lake level and Pleistocene climate fluctuations. Ecol Evol 6:656–674. https://doi.org/10.1002/ece3.1890
Hu Z, Uwai S, Yu S, Komatsu T, Ajisaka T, Duan D (2011) Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol 20:3894–3909. https://doi.org/10.1111/j.1365-294X.2011.05220.x
Kai Z, Li J, Yang G, Duan Z, He S (2005) Molecular phylogenetics of Gymnocypris (Teleostei: Cyprinidae) in Lake Qinghai and adjacent drainages. Sci Bull 50:1326–1334
Kenthao A, Wangsomnuk P, Jearranaiprepame P (2018) Genetic variations and population structure in three populations of beardless barb, Cyclocheilichthys apogon (Valenciennes, 1842) inferred from mitochondrial cytochrome b sequences. Mitochondrial DNA A DNA Mapp Seq Anal 29:82–90. https://doi.org/10.1080/24701394.2016.1242581
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016:054
Liang Y, He D, Jia Y, Sun H, Chen Y (2017) Phylogeographic studies of schizothoracine fishes on the central Qinghai-Tibet Plateau reveal the highest known glacial microrefugia. Sci Rep 7:10983
Mamiatis T, Fritsch E, Sambrook J, Engel J (2010) Molecular cloning—a laboratory manual. New York: cold spring harbor laboratory. 1982, 545s. Acta Biotechnol 5:104
Meyer M, Hoffmann D, Aldenderfer M, Haas W, Dahl J, Wang Z, Degering D, Schlütz F (2017) Permanent human occupation of the central Tibetan Plateau in the early Holocene. Science 355:64–67
Molnar P, England P, Martinod J (1993) Mantle dynamics, uplift of the Tibetan Plateau, and the Indian Monsoon. Rev Geophys 31:357
Morcillo F, Ornelas C, Alcaraz L, Matamoros W, Doadrio I (2016) Phylogenetic relationships and evolutionary history of the Mesoamerican endemic freshwater fish family Profundulidae (Cyprinodontiformes: Actinopterygii). Mol Phylogenet Evol 94:242–251. https://doi.org/10.1016/j.ympev.2015.09.002
Ni P, Bhuiyan A, Chen J, Li J, Zhang C, Zhao S et al (2018) De novo assembly of mitochondrial genomes provides insights into genetic diversity and molecular evolution in wild boars and domestic pigs. Genetica 146:277–285. https://doi.org/10.1007/s10709-018-0018-y
Noda A, Yonesaka R, Sasazaki S, Mannen H (2018) The mtDNA haplogroup P of modern Asian cattle: a genetic legacy of Asian aurochs? PLoS ONE 13:e0190937. https://doi.org/10.1371/journal.pone.0190937
O'Bryan D, Xie Z, Wang Y, Du J, Brauner C, Richards J et al (2010) Phylogeography and conservation genetics of Lake Qinghai scaleless carp Gymnocypris przewalskii. J Fish Biol 77:2072–2092. https://doi.org/10.1111/j.1095-8649.2010.02792.x
Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic difference. Mol Biol Evol 9:552–569
Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18:169–185. https://doi.org/10.1111/j.1365-294X.2008.03981.x
Schneider S, Excoffer L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Steinke D, Salzburger W, Braasch I, Meyer A (2006) Many genes in fish have species-specific asymmetric rates of molecular evolution. BMC Genom 7:20. https://doi.org/10.1186/1471-2164-7-20
Su J, Ji W, Wei Y, Zhang Y, Gleeson D, Lou Z, Ren J (2014) Genetic structure and demographic history of the endangered and endemic schizothoracine fish Gymnodiptychus pachycheilus in Qinghai-Tibetan Plateau. Zool Sci 31:515–522. https://doi.org/10.2108/zs130238
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595. https://doi.org/10.0000/PMID2513255
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035
Tamura K, Battistuzzi F, Billing P, Murillo O, Filipski A, Kumar S (2012) Estimating divergence times in large molecular phylogenies. Proc Natl Acad Sci 109:19333–19338
Templeton A (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397
Tong C, Tian F, Tang Y, Feng C, Guan L, Zhang C, Zhao K (2016) Positive Darwinian selection within interferon regulatory factor genes of Gymnocypris przewalskii (Cyprinidae) on the Tibetan Plateau. Fish Shellfish Immunol 50:34–42
Tong C, Fei T, Zhang C, Zhao K (2017) Comprehensive transcriptomic analysis of Tibetan Schizothoracinae fish Gymnocypris przewalskii reveals how it adapts to a high altitude aquatic life. BMC Evol Biol 17:74
Venkatesh B (2003) Evolution and diversity of fish genomes. Curr Opin Genet Dev 13:588–592. https://doi.org/10.1016/j.gde.2003.09.001
Wang M, Sheng Z, Wu X, Wang Q, Pan Y (2010) Mitochondrial DNA-based genetic structure analysis of Pudong White pigs. Biochem Genet 48:924–937. https://doi.org/10.1007/s10528-010-9373-9
Wang X, Gan X, Li J, Chen Y, He S (2016) Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau. Sci China Life Sci 59:1149–1165. https://doi.org/10.1007/s11427-016-0007-7
Wang W, Zheng W, Zhang P, Li Q, Kirby E, Yuan D et al (2017) Expansion of the Tibetan Plateau during the Neogene. Nat Commun 8:15887. https://doi.org/10.1038/ncomms15887
Wu Y, Wu C (1992) The fishes of the Qinghai-Xizang plateau. Sichuan Publishing House of Science & Technology, Sichuan, pp 23–27
Wu G, Yao Y, Qu K, Ding Z, Li H, Palanichamy M et al (2007) Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol 8:R245. https://doi.org/10.1186/gb-2007-8-11-r245
Xiao T, Lu C, Li C, Zhang M (2013) Genetic diversity and phylogenetic analysis of eight Cyprinoid aquaculture breeds based on mitochondrial Cyt b gene. J Fish China 37:344–350
Xie ZY, Du JZ, Chen XQ, Wang YX, Murray BW (2006) The significance of mitochondria control region (D-Loop) in intraspecific genetic differentiation of fish. Hereditas 28:362–368
Yang Y, Gao Y, Wang S, Xu D, Yu H, Wu L et al (2014) The microbial gene diversity along an elevation gradient of the Tibetan grassland. ISME J 8:430–440. https://doi.org/10.1038/ismej.2013.146
Yuan B, Chen K, Bowler J (1990) The formation and evolution of the Qinghai Lake. Quat Sci 10:233–243
Zhang F, Jiang Z (2006) Mitochondrial phylogeography and genetic diversity of Tibetan gazelle (Procapra picticaudata): implications for conservation. Mol Phylogenet Evol 41:313–321. https://doi.org/10.1016/j.ympev.2006.05.024
Zhang Y, Jiang P, Gang H, Shi J, Sun X (2009) Development and characterization of microsatellite markers to study population genetic diversity of Przewalski's naked carp Gymnocypris przewalskii in China. J Fish Biol 75:2352–2356. https://doi.org/10.1111/j.1095-8649.2009.02437.x
Zhang R, Peng Z, Li G, Zhang C, Tang Y, Gan X, He S, Zhao K (2013) Ongoing speciation in the Tibetan Plateau Gymnocypris species complex. PLoS ONE 8:e71331
Zhang J, Liu Z, Zhang B, Yin X, Wang L, Shi H, Kang Y (2015a) Genetic diversity and taxonomic status of Gymnocypris chilianensis based on the mitochondrial DNA cytochrome b gene. Genet Mol Res 14(3):9253–9260. https://doi.org/10.4238/2015.August.10.5
Zhang R, Ludwig A, Zhang C, Tong C, Li G, Tang Y et al (2015b) Local adaptation of Gymnocypris przewalskii (Cyprinidae) on the Tibetan Plateau. Sci Rep 5:9780. https://doi.org/10.1038/srep09780
Zhang J, Jiao T, Zhao S (2016) Genetic diversity in the mitochondrial DNA D-loop region of global swine (Sus scrofa) populations. Biochem Biophys Res Commun 473:814–820. https://doi.org/10.1016/j.bbrc.2016.03.125
Zhang D, Yu M, Hu P, Peng S, Liu Y, Li W et al (2017) Genetic adaptation of schizothoracine fish to the phased uplifting of the Qinghai-Tibetan Plateau. G3 (Bethesda) 7:1267–1276. https://doi.org/10.1534/g3.116.038406
Zhao K, Duan Z, Yang G, Peng Z, He S, Chen Y (2007) Origin of Gymnocypris przewalskii and phylogenetic history of Gymnocypris eckloni (Teleostei: Cyprinidae). Prog Nat Sci 17:520–528
Zhao K, Duan Z, Peng Z, Guo S, Li J, He S, Zhao X (2009) The youngest split in sympatric schizothoracine fish (Cyprinidae) is shaped by ecological adaptations in a Tibetan Plateau glacier lake. Mol Ecol 18:3616–3628. https://doi.org/10.1111/j.1365-294X.2009.04274.x
Zhao K, Duan Z, Peng Z (2011) Phylogeography of the endemic Gymnocypris chilianensis (Cyprinidae): sequential westward colonization followed by allopatric evolution in response to cyclical Pleistocene glaciations on the Tibetan Plateau. Mol Phylogenet Evol 59:303–310
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The study was supported by the Natural Science Foundation of Gansu Province (1506 RJZA025). The funding bodies had no role in the design of the study; the collection, analysis, and interpretation of the data; or the writing of the manuscript.
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JQ and ZL2 conceived and designed the experiments. JQ, GZ, LL, JZ and ZL1 performed the experiments. JQ, GZ and LL analyzed the data. YK and ZL2 contributed reagents, materials and tools and collected the samples. JQ and ZL2 wrote the manuscript and revised the manuscript. All authors read and approved the final manuscript.
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Additional file 1:
Information for 281 Gymnocypris species (XLSX 15 kb)
Additional file 2:
Distribution and frequencies of 188 haplotypes from 281 Gymnocypris species (XLSX 19 kb)
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Quan, J., Zhao, G., Li, L. et al. Phylogeny and genetic diversity reveal the influence of Qinghai-Tibet Plateau uplift on the divergence and distribution of Gymnocypris species. Aquat Sci 83, 6 (2021). https://doi.org/10.1007/s00027-020-00761-9
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DOI: https://doi.org/10.1007/s00027-020-00761-9