BMC Evolutionary Biology | |
Geological events and Pliocene climate fluctuations explain the phylogeographical pattern of the cold water fish Rhynchocypris oxycephalus (Cypriniformes: Cyprinidae) in China | |
Huanzhang Liu1  Xiaojuan Li1  Qiongying Tang1  Ming Chen1  Dan Yu1  | |
[1] The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P.R. China | |
关键词: Conservation; Neogene climate fluctuations; Three steps; Cryptic subspecies; Phylogeography; | |
Others : 1117862 DOI : 10.1186/s12862-014-0225-9 |
|
received in 2014-07-01, accepted in 2014-10-17, 发布年份 2014 | |
【 摘 要 】
Background
Rhynchocypris oxycephalus is a cold water fish with a wide geographic distribution including the relatively warm temperate regions of southern China. It also occurs in second- and third-step geomorphic areas in China. Previous studies have postulated that high-altitude populations of R. oxycephalus in southern China are Quaternary glacial relics. In this study, we used the mitochondrial gene Cytb and the nuclear gene RAG2 to investigate the species phylogeographical patterns and to test two biogeographic hypotheses: (1) that divergence between lineages supports the three-step model and (2) climatic fluctuations during the Quaternary resulted in the present distribution in southern China.
Results
Phylogenetic analysis detected three major matrilines (A, B, and C); with matrilines B and C being further subdivided into two submatrilines. Based on genetic distances and morphological differences, matriline A potentially represents a cryptic subspecies. The geographic division between matrilines B and C coincided with the division of the second and third geomorphic steps in China, suggesting a historical vicariance event. Pliocene climatic fluctuations might have facilitated the southwards dispersal of R. oxycephalus in matriline C, with the subsequent warming resulting in its split into submatrilines C1 and C2, leaving submatriline C2 as a relic in southern China.
Conclusions
Our study demonstrates that geological events (three steps orogenesis) and climate fluctuations during the Pliocene were important factors in shaping phylogeographical patterns in R. oxycephalus. Notably, no genetic diversity was detected in several populations, all of which possessed unique genotypes. This indicates the uniqueness of local populations and calls for a special conservation plan for the whole species at the population level.
【 授权许可】
2014 Yu et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150206011246248.pdf | 1585KB | download | |
Figure 4. | 17KB | Image | download |
Figure 3. | 31KB | Image | download |
Figure 2. | 36KB | Image | download |
Figure 1. | 154KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Mayr E: Systematics and the Origin of Species. Columbia University Press, New York; 1942.
- [2]Rundle HD, Nosil P: Ecological speciation. Ecol Lett 2005, 8:336-352.
- [3]Liu JQ, Wang YJ, Wang AL, Hideaki O, Abbott RJ: Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Mol Phylogenet Evol 2006, 38:31-49.
- [4]Che J, Zhou WW, Hu JS, Yan F, Papenfuss TJ, Wake DB, Zhang YP: Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci U S A 2010, 107:13765-13770.
- [5]Li ZJ, Yu GH, Rao DQ, Yang JX: Phylogeography and demographic history of Babina pleuraden (Anura, Ranidae) in southwestern China. PLoS ONE 2012, 7:e34013.
- [6]Jiang F, Wu X: Fundamental characteristics of the stepped landform in China continent. Mar Geol & Quat Ge 1993, 13:15-24.
- [7]Yuan QJ, Zhang ZY, Peng H, Ge S: Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in Southwest China and northern Vietnam. Mol Ecol 2008, 17:1054-1065.
- [8]Yan J, Wang QX, Chang Q, Ji X, Zhou K: The divergence of two independent lineages of an endemic Chinese gecko, Gekko swinhonis, launched by the Qinling orogenic belt. Mol Ecol 2010, 19:2490-2500.
- [9]Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF: Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 1998, 7:453-464.
- [10]Hewitt GM: Genetic consequences of climatic oscillations in the Quaternary. Philos T Roy Soc B 2004, 359:183-195.
- [11]Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS: Comparative phylogeography of unglaciated eastern North America. Mol Ecol 2006, 15:4261-4293.
- [12]Hewitt G: The genetic legacy of the Quaternary ice ages. Nature 2000, 405:907-913.
- [13]Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR: Global vegetation change through the Miocene/Pliocene boundary. Nature 1997, 389:153-158.
- [14]Zachos J, Pagani M, Sloan L, Thomas E, Billups K: Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 2001, 292:686-693.
- [15]Wu Y, Wang Y, Jiang K, Hanken J: Significance of pre-Quaternary climate change for montane species diversity: insights from Asian salamanders (Salamandridae: Pachytriton). Mol Phylogenet Evol 2013, 66:380-390.
- [16]Miralles A, Carranza S: Systematics and biogeography of the Neotropical genus Mabuya, with special emphasis on the Amazonian skink Mabuya nigropunctata (Reptilia, Scincidae). Mol Phylogenet Evol 2010, 54:857-869.
- [17]Huang PH: Quaternary climatic changes in china and problem of Lushan glaciation remnants. J Glaciol Geocryol 1982, 4:1-14.
- [18]Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sanchez-Azofeifa GA, Still CJ, Young BE: Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 2006, 439:161-167.
- [19]Milanovich JR, Peterman WE, Nibbelink NP, Maerz JC: Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. Plos ONE 2010, 5:10.
- [20]Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE: Extinction risk from climate change. Nature 2004, 427:145-148.
- [21]Wake DB: Facing extinction in real time. Science 2012, 335:1052-1053.
- [22]Bogutskaya NG, Naseka AM, Shedko SV, Vasil’eva ED, Chereshnev IA: The fishes of the Amur River: updated check-list and zoogeography. Ichthyol Explor Fres 2008, 19:301-366.
- [23]Jang MH, Kim JG, Park SB, Jeong KS, Cho G, Joo G: The current status of the distribution of introduced fish in large river systems of South Korea. Int Rev Hydrobiol 2002, 87:319-328.
- [24]Yu D, Chen M, Zhou ZC, Eric R, Tang QY, Liu HZ: Global climate change will severely decrease potential distribution of the East Asian coldwater fish Rhynchocypris oxycephalus (Actinopterygii, Cyprinidae). Hydrobiologia 2013, 700:23-32.
- [25]Zhang E, Chen YY: Fish Fauna in Northeastern Jiangxi Province with a discussion on the zoogeographical division of East China. Acta Hydrobiologica Sinca 1997, 3:254-261. (in Chinese)
- [26][http://commons.wikimedia.org/wiki/File:East_Asia_topographic_map.png] webcite Wikimedia Commons. []
- [27]Tang Q, Freyhof J, Xiong B, Liu H: Multiple invasions of Europe by East Asian cobitid loaches (Teleostei: Cobitidae). Hydrobiologia 2008, 605:17-28.
- [28]Doadrio I, Carmona JA, Machordom A: Haplotype diversity and phylogenetic relationships among the Iberian Barbels (Barbus, Cyprinidae) reveal two evolutionary lineages. J Hered 2002, 93:140-147.
- [29]Hansen JD, Kaattari SL: The recombination activating gene 2 (RAG2) of the rainbow trout Oncorhynchus mykiss. Immunogenetics 1996, 44:203-211.
- [30]Willett CE, Cherry JJ, Steiner LA: Characterization and expression of the recombination activating genes (rag1 and rag2) of zebrafish. Immunogenetics 1997, 45:394-404.
- [31]Kim KY, Ko MH, Liu H, Tang QY, Chen XL, Miyazaki J, Bang I: Phylogenetic relationships of Pseudorasbora, Pseudopungtungia, and Pungtungia (Teleostei; Cypriniformes; Gobioninae) inferred from multiple nuclear gene sequences. BioMed Res Int 2013, 2013:Article ID 347242, 6 pages.
- [32]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882.
- [33]Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics 1996, 12:543-548.
- [34]Swofford DL: PAUP*: Phylogenetic Analysis using Parsimony (* and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts; 2002.
- [35]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
- [36]Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population Data. Am J Hum Genet 2001, 68:978-989.
- [37]Flot JF: SeqPHASE: a web tool for interconverting phase input/output files and FASTA sequence alignments. Mol Ecol Resour 2010, 10:162-166.
- [38]Woerner AE, Cox MP, Hammer MF: Recombination-filtered genomic datasets by information maximization. Bioinformatics 2007, 23:1851-1853.
- [39]Librado P, Rozas J: Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
- [40]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9:772.
- [41]Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biol 2003, 52:696-704.
- [42]Ronquist F, Huelsenbeck JP: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
- [43]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Sys Biol 2010, 59:307-321.
- [44]Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
- [45]Takezaki N, Rzhetsky A, Nei M: Phylogenetic tests of the molecular clock and linearized trees. Mol Biol Evol 1995, 12:823-833.
- [46]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
- [47]Durand JD, Tsigenopoulos CS, Unlü E, Berrebi P: Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from Cytochrome b DNA–evolutionary significance of this region. Mol Phylogenet Evol 2002, 22:91-100.
- [48]Ketmaier V, Bianco PG, Cobolli M, Krivokapic M, Caniglia R, De Matthaeis E: Molecular phylogeny of two lineages of Leuciscinae cyprinids (Telestes and Scardinius) from the peri-Mediterranean area based on Cytochrome b data. Mol Phylogenet Evol 2004, 32:1061-1071.
- [49]Tang Q, Liu S, Yu D, Liu H, Patrick D: Mitochondrial capture and incomplete lineage sorting in the diversification of balitorine loaches (Cypriniformes, Balitoridae) revealed by mitochondrial and nuclear genes. Zool Scr 2012, 41:233-247.
- [50]Meyer A: Evolution of Mitochondrial DNA in Fishes. In Biochemistry and Molecular Biology of Fishes, Volume 2. Edited by Hochachka PW, Mommsen TP. Elsevier, Hague; 1993:1-38.
- [51][http://beast.bio.ed.ac.uk/Tracer] webcite Rambaut A, Drummond AJ: Tracer v1.4. []
- [52][http://tree.bio.ed.ac.uk/software/figtree/] webcite Rambaut A: FigTree. []
- [53]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
- [54]Tajima F: Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
- [55]Fu YX: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
- [56]Slatkin M, Hudson RR: Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 1991, 1991(129):555-562.
- [57]Rogers AR, Harpending H: Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 1992, 9:552-569.
- [58]Heled J, Drummond AJ: Bayesian inference of population size history from multiple loci. BMC Evol Biol 2008, 8:289. BioMed Central Full Text
- [59]Chen YY: Fauna Sinica. Osteichthyes. Cypriniformes II. Sciences Press, Beijing; 1998.
- [60]Hosoya K: Cyprinidae. In Fishes of Japan with Pictorial Keys to the Species. 2nd edition. Edited by Nakabo T. Tokai University Press, Tokyo; 2000.
- [61]McPhail JD, Taylor EB: Morphological and genetic variation in northwestern suckers, Castosomus Catostomus: The salish sucker problem. Copeia 1999, 1999:884-892.
- [62]Chang MM, Chen YY, Tong HW: A new Miocene Xenocyprinine (Cyprinidae) from Heilongjiang Province, Northeast China and succession of late Cenozoic fish faunas of East Asia. Vertebrata Palasiatica 1996, 34:165-183.
- [63]Kartavtsev YP: Divergence at Cyt-b and Co-1 mtDNA genes on different taxonomic levels and genetics of speciation in animals. Mitochondrial DNA 2011, 22:55-65.
- [64]Zhang LS: Palaeogeography of China. Science Press, Beijing; 2012.
- [65]Zhang DF, Feng QL, Jian MB: Eco-environmental effects of the Qinghai-Tibet Plateau uplift during the Quaternary in China. Environ Geol 2000, 39:1352-1357.
- [66]He SP, Cao WX, Chen YY: The uplift of Qinghai-Xizang (Tibet) Plateau and the vicariance speciation of glyptosternoid fishes (Siluriformes: Sisoridae). Sci China C Life Sci 2001, 44:644-651.
- [67]Zhang DR, Chen MY, Murphy RW, Che J, Pang JF, Hu JS, Luo J, Wu SJ, Ye H, Zhang YP: Genealogy and palaeodrainage basins in Yunnan Province: phylogeography of the Yunnan spiny frog, Nanorana yunnanensis (Dicroglossidae). Mol Ecol 2010, 19:3406-3420.
- [68]He DK, Chen YF: Molecular phylogeny and biogeography of the highly specialized grade schizothoracine fishes (Teleostei: Cyprinidae) inferred from cytochrome b sequences. Chinese Sci Bull 2007, 52:777-788.
- [69]Ravelo AC, Andreasen DH, Lyle M, Lyle AO, Wara MW: Regional climate shifts caused by gradual global cooling in the Pliocene epoch. Nature 2004, 429:263-267.
- [70]Salzmann U, Williams M, Haywood AM, Johnson ALA, Kender S, Zalasiewicz J: Climate and environment of a Pliocene warm world. Palaeogeogr Palaeocl 2011, 309:1-8.
- [71]Hodell DA, Elmstrom KM, Kennett JP: Latest Miocene benthic δ18O changes, global ice volume, sea level and the ‘Messinian salinity crisis’. Nature 1986, 320:411-414.
- [72]Salzmann U, Dolan A, Haywood A, Chan WL, Voss J, Hill D, Abe-Ouchi A, Bragg F, Chandler M, Contoux C, Dowsett H, Jost A, Kamae Y, Lohmann G, Lunt D, Pickering S, Pound M, Ramstein G, Sohl L, Stepanek S, Ueda H, Zhang Z: Challenges in quantifying Pliocene terrestrial warming revealed by data–model discord. Nat Clim Change 2013, 3:969-974.
- [73]Pfrender ME, Hicks J, Lynch M: Biogeographic patterns and current distribution of molecular-genetic variation among populations of speckled dace, Rhinichthys osculus (Girard). Mol Phylogenet Evol 2004, 30:490-502.
- [74]Yan F, Zhou W, Zhao H, Yuan Z, Wang Y, Jiang K, Jin J, Murphy RW, Che J, Zhang Y: Geological events play a larger role than Pleistocene climatic fluctuations in driving the genetic structure of Quasipaa boulengeri (Anura: Dicroglossidae). Mol Ecol 2013, 22:1120-1133.
- [75]Chung MY, Lopez-Pujol J, Maki M, Kim KJ, Chung JM, Sun BY, Chung MG: Genetic diversity in the common terrestrial orchid Oreorchis patens and its rare congener Oreorchis coreana: inference of species evolutionary history and implications for conservation. J Hered 2012, 103:692-702.
- [76]Frankham R, Ballou JD, Briscoe DA: Introduction to Conservation Genetics. Cambridge University Press, Cambridge; 2002.