Abstract
Drainage development and climatic fluctuations shape the phylogeographic patterns of freshwater fish species. In this study, we used the mitochondrial control region to determine the population structure and demographical history of the leopard mandarin fish (Siniperca scherzeri) in the Pearl River drainage and to test whether the historical development of the river and climatic changes that occurred in southern China have influenced the phylogeographic patterns of this species. Phylogenetic analyses, the use of haplotype networks, and population structure analyses revealed two geographically distinct genetic lineages, A and B. Lineage A was widespread in the Xijiang and Beijiang Rivers, whereas lineage B was only detected in the Dongjiang River. Dating analyses and biogeographic analyses indicated that the two lineages originated from a vicariance event 1.11 million years ago (Ma), which coincides with the historical development of the drainage during the early Quaternary period. Demographic analyses showed that the populations of lineage B experienced sharp demographic contraction of 0.01 Ma, which suggests that sea-level transgression after the Last Glacial Maximum may have played a critical role in the population demography of lineage B. By contrast, the populations of lineage A were less influenced by the sea-level transgression owing to larger distribution ranges. Overall, our study uncovered the phylogeographic patterns of Siniperca scherzeri in the Pearl River drainage and provides valuable information for the management and conservation of this species.
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Data availability
Novel DNA sequences presented in this study have been submitted to GenBank with accession numbers of OL330809–OL330973.
References
Barrett JC, Fry B, Maller J, Daly MJ (2004) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265. https://doi.org/10.1093/bioinformatics/bth457
Buhay JE, Crandall KA (2005) Subterranean phylogeography of freshwater crayfishes shows extensive gene flow and surprisingly large population sizes. Mol Ecol 14:4259–4273. https://doi.org/10.1111/j.1365-294X.2005.02755.x
Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25(4):624–633. https://doi.org/10.1093/molbev/msm271
Cao L, Liang XF, Du Y, Zheng H, Yang M, Huang W (2013) Genetic population structure in Siniperca scherzeri (Perciformes: Siniperca) in China inferred from mitochondrial DNA sequences and microsatellite loci. Biochem Syst Ecol 51:160–170. https://doi.org/10.1016/j.bse.2013.08.024
Chen W, Li C, Chen F, Li Y, Yang J, Li J, Li X (2020) Phylogeographic analyses of a migratory freshwater fish (Megalobrama terminalis) reveal a shallow genetic structure and pronounced effects of sea-level changes. Gene 737:144478. https://doi.org/10.1016/j.gene.2020.144478
Chen XL, Chiang TY, Lin HD, Zheng HS, Shao KT, Zhang Q, Hsu KC (2007) Mitochondrial DNA phylogeography of Glyptothorax fokiensis and Glyptothorax hainanensis in Asia. J Fish Biol 70:75–93. https://doi.org/10.1111/j.1095-8649.2007.01370.x
Chen Y, Cao W, Zheng C (1986) Ichthyofauna of the Zhujiang River with a discussion on zoogeographical divisions for freshwater fishes. Acta Hydrobiologica Sinica 10:228–236. http://ir.ihb.ac.cn/handle/152342/6328
Chiang TY, Lin HD, Zhao J, Kuo PH, Lee TW, Hsu KC (2013) Diverse processes shape deep phylogeographical divergence in Cobitis sinensis (Teleostei: Cobitidae) in East Asia. J Zool Syst Evol Res 51(4):316–326. https://doi.org/10.1111/jzs.12030
Donaldson KA, Wilson RR (1999) Amphi-panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 13(1):208–213. https://doi.org/10.1006/mpev.1999.0625
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11(12):2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 35: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2):479–491. https://doi.org/10.1093/genetics/131.2.479
Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66(2):95–107. https://doi.org/10.1017/S0016672300034455
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925. https://doi.org/10.1093/genetics/147.2.915
Gascoyne M, Benjamin GJ, Schwarcz HP, Ford DC (1979) Sea-level lowering during the illinoian glaciation: evidence from a bahama “blue hole.” Science 205(4408):806. https://doi.org/10.1126/science.205.4408.806
Huey JA, Cook BD, Unmack PJ, Hughes JM (2013) Broadscale phylogeographic structure of five freshwater fishes across the Australian Monsoonal Tropics. Freshw Sci 33(1):273–287. https://doi.org/10.1086/674984
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–20. https://doi.org/10.1007/BF01731581
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Liu KB (1988) Quaternary history of the temperate forests of China. Quaternary Sci Rev 7(1):1–20. https://doi.org/10.1016/0277-3791(88)90089-3
Nylander J (2004) MrModeltest v2. Program distributed by the author (ed. Nylander JAA). Evolutionary Biology Centre, Uppsala University, Uppsala
Pearse DE, Crandall K (2004) Beyond FST: analysis of population genetic data for conservation. Conserv Genet 5:585–602. https://doi.org/10.1007/s10592-003-1863-4
Perea S, Doadrio I (2015) Phylogeography, historical demography and habitat suitability modelling of freshwater fishes inhabiting seasonally fluctuating Mediterranean river systems: a case study using the Iberian cyprinid Squalius valentinus. Mol Ecol 24(18):4808. https://doi.org/10.1111/mec.13274
Qiu C, Lin Y, Qing N, Zhao J, Chen X (2008) Genetic variation and phylogeography of Micronoemacheilus pulcher populations among drainage systems between western South China and Hainan Island. Acta Entomol Sin 51(5):1099–1128. https://doi.org/10.1063/1.2964478
Rambaut A, Drummond A (2007) Tracer v1.4. Available at: http://beast.bio.ed.ac.uk/Tracer
Rincon-Sandoval M, Betancur-R R, Maldonado-Ocampo JA (2019) Comparative phylogeography of trans-Andean freshwater fishes based on genome-wide nuclear and mitochondrial markers. Mol Ecol 28(5):1096–1115. https://doi.org/10.1111/mec.15036
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Shi YF, Ren BH, Wang JT, Derbyshire E (1986) Quaternary glaciation in China. Quaternary Sci Rev 5:503–507. https://doi.org/10.1016/0277-3791(86)90217-9
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690
Swartz ER, Skelton PH, Bloomer P (2007) Sea-level changes, river capture and the evolution of populations of the Eastern Cape and fiery redfins (Pseudobarbus afer and Pseudobarbus phlegethon, Cyprinidae) across multiple river systems in South Africa. J Biogeogr 34(12):2086–2099. https://doi.org/10.1111/j.1365-2699.2007.01768.x
Swofford DL (2002) PAUP* 4.0 b10: Phylogenetic analysis using parsimony. Sinauer Associates, Sunderland, Massachusetts
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 60. Mol Biol Evol 30(12):2725–2759. https://doi.org/10.1093/molbev/mst197
Wang L, Sarnthein M, Erlenkeuser H, Grimalt J, Grootes P, Heilig S, Ivanova E, Kienast M, Pelejero C, Pflaumann U (1999) East Asian monsoon climate during the Late Pleistocene: high-resolution sediment records from the South China Sea. Mar Geol 156(1–4):245–284. https://doi.org/10.1016/S0025-3227(98)00182-0
Wang P, Li Q (2009) The South China Sea: paleoceanography and sedimentology. Springer, Dordrecht
Wang W, Zhao J, Li S (2006) Genetic variation of the mitochondrial DNA cyt b among six populations of Siniperca scherzeri in China. Zool Res 27(6): 589–593
Wang WW, Zhao JL, Li SF, Wang CJ (2009) Genetic variation of Siniperca scherzeri steindachner from different geographical populations by AFLP analysis. Acta Hydrobiol Sin 33(2):304–309. https://doi.org/10.3724/SP.J.0000.2009.20304
Wong W, Ma K, Tsang L, Chu K (2017) Genetic legacy of tertiary climatic change: a case study of two freshwater loaches, Schistura fasciolata and Pseudogastromyzon myersi. Hong Kong Heredity 119(5):360. https://doi.org/10.1038/hdy.2017.47
Wu TH, Tsang LM, Chen IS, Chu KH (2016) Multilocus approach reveals cryptic lineages in the goby Rhinogobius duospilus in Hong Kong streams: role of paleodrainage systems in shaping marked population differentiation in a city. Mol Phylogenet Evol 104:112–122. https://doi.org/10.1016/j.ympev.2016.07.014
Xiao W, Zhang Y, Liu H (2001) Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Mol Phylogenet Evol 18(2):163–173. https://doi.org/10.1006/mpev.2000.0879
Yang L, He S (2008) Phylogeography of the freshwater catfish Hemibagrus guttatus (Siluriformes, Bagridae): implications for South China biogeography and influence of sea-level changes. Mol Phylogenet Evol 49(1):393–398. https://doi.org/10.1016/j.ympev.2008.05.032
Yang L, Mayden RL, He S (2009) Population genetic structure and geographical differentiation of the Chinese catfish Hemibagrus macropterus (Siluriformes, Bagridae): evidence for altered drainage patterns. Mol Phylogenet Evol 51(2):405–411. https://doi.org/10.1016/j.ympev.2009.01.004
Yu Y, Harris AJ, Blair C, He XJ (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol 87:46–49. https://doi.org/10.1016/j.ympev.2015.03.008
Zhang H (1990) Newly neotectonic movement and geological environment along the Coast of South China. Seismological press, Beijing
Zhang HN, Chen CG, Huang KR, Li ZQ, Zhang FL, Chen GZ (1990) The new geological structures, tectonic movements and geological environment in coastal line of South China. Earthquake press, Beijing
Zheng C (1989) Ichthyography of the Pearl River. Science Press, Beijing
Zhou J, Zhang C (2005) Freshwater Fishes of Guangxi. China. Guangxi People’s Publishing House, Nanning
Zong Y, Yim WS, Yu F, Huang G (2009) Late Quaternary environmental changes in the Pearl River mouth region. China Quatern Int 206(1–2):35–45. https://doi.org/10.1016/j.quaint.2008.10.012
Acknowledgements
We thank Natalie Kim, PhD, from Liwen Bianji (Edanz) (www.liwenbianji.cn/) for editing the English text of a draft of this manuscript.
Funding
This work was supported by the China Agriculture Research System (CARS-46), China-ASEAN Maritime Cooperation Fund (CAMC-2018F), and National Freshwater Genetic Resource Center (NFGR-2020).
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Conceptualization: X.L. and Y.D.; methodology: M.L., X.L., J.G.; software: M.L., X.L., J.G.; validation: M.L., X.L., J.G.; formal analysis: M.L., X.L.; investigation: M.L., X.L., J.G., Y.D., Y.K., Q.Z.; resources: X.L., J.G., Y.D., Y.K., Q.Z.; data curation: M.L., X.L.; writing—original draft preparation: M.L., X.L.; writing—review and editing: M.L., X.L., J.G., Y.D., Y.K., Q.Z.; visualization: M.L., X.L., J.G.; supervision: X.L., J.G., Y.D.; project administration: M.L., X.L., J.G.; funding acquisition: M.L., X.L. All authors have read and agreed to the published version of the manuscript.
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Lin, M., Liang, X., Gao, J. et al. Phylogeographic structure and population demography of the leopard mandarin fish (Siniperca scherzeri) in the Pearl River drainage. Environ Biol Fish 105, 477–486 (2022). https://doi.org/10.1007/s10641-022-01247-3
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DOI: https://doi.org/10.1007/s10641-022-01247-3