Abstract
The rosy bitterling, Rhodeus ocellatus, is a small freshwater fish belonging to the family Cyprinidae. This species lives in ponds where freshwater mussels are abundant and female lays eggs inside mussels. To understand whether the reproduction mode influenced the phylogeography, our study examined the genetic structure of R. ocellatus using sequences from the mitochondrial DNA (cytochrome b gene and control region) and nuclear DNA (the first intron of ribosomal protein S7 gene). In total, 213 specimens were collected from twelve populations in south of Yangtze River, including Yangtze River, Taiwan and Hainan Islands. The phylogenetic analyses based on mitochondrial and nuclear sequences both showed the lack of a population genetic structure, but all results, including the approximate Bayesian computation approaches, showed that these two markers revealed incongruent historical signals. Our study found that (1) the discordance between these two markers were accounted for admixtures by introduced; (2) the phylogeographic pattern of R. ocellatus and that of other freshwater fish were identical; (3) the reproduction mode was due to that the gene flows among populations were limited; and (4) R. ocellatus colonized in south of the Yangtze River (including) after southeast coastal districts formed and before Taiwan Island reached its present shape by comparing our results with that of the previous studies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13(4):729–744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Ballard JW, Chernoff B, James AC (2002) Divergence of mitochondrial DNA is not corroborated by nuclear DNA, morphology, or behavior in Drosophila simulans. Evolution 56(3):527–545. https://doi.org/10.1111/j.0014-3820.2002.tb01364.x
Berrebi P, Retif A, Fang F, Zhang CG (2006) Population structure and systematics of Opsariichthys bidens (Osteichthyes: Cyprinidae) in south-east China using a new nuclear marker: the introns (EPIC-PCR). Biol J Linn Soc 87(1):155–166. https://doi.org/10.1111/j.1095-8312.2006.00563.x
Brito PH (2007) Contrasting patterns of mitochondrial and microsatellite genetic structure among western European populations of tawny owls (Strix aluco). Mol Ecol 16(16):3423–3437. https://doi.org/10.1111/j.1365-294X.2007.03401.x
Chen XL, Chiang TY, Lin HD, Zheng HS, Shao KT, Zhang Q, Hsu KC (2007) Mitochondrial DNA phylogeographyof Glyptothorax fokiensis and Glyptothorax hainanensis in Asia. J Fish Biol 70(sa):75–93. https://doi.org/10.1111/j.1095-8649.2007.01370.x
Chiang TY, Lin HD, Shao KT, Hsu KC (2010) Multiple factors have shaped the phylogeography of Chinese spiny loach (Cobitis sinensis) in Taiwan as inferred from mitochondrial DNA variation. J Fish Biol 76(5):1173–1189. https://doi.org/10.1111/j.1095-8649.2010.02589.x
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 51:316–326
Chiang TY, Chen YY, Lee TW, Hsu KC, Lin FJ, Wang WK, Lin HD (2017) Comparative phylogeography of two codistributed endemic cyprinids in southeastern Taiwan. Biochem Syst Ecol 70:283–290. https://doi.org/10.1016/j.bse.2016.12.010
Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7(9):1255–1256
Clark MK, Schoenbohm LM, Royden LH, Whipple KX, Burchfiel BC, Zhang X, Tang W, Wang E, Chen L (2004) Surface uplift, tectonics, and erosion of eastern Tibet from large scale drainage patterns. Tectonics 23:TC106
Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Estoup A (2014) DIYABC v2. 0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189
Crochet PA (2000) Genetic structure of avian populations—allozymes revisited. Mol Ecol 9(10):1463–1469. https://doi.org/10.1046/j.1365-294x.2000.01026.x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772. https://doi.org/10.1038/nmeth.2109
Drummond AJ, Rambau A, Suchard M (2013) BEAST:1.8.0 http://beast.bio.ed.ac.uk
Dupanloup I, Schneidera S, Excoffier NL (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: 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
Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the younger Dryas event and deep-ocean circulation. Nature 342(6250):637–642. https://doi.org/10.1038/342637a0
Froese R, Pauly D (2017) FishBase. World Wide Web electronic publication http://www.fishbase.org
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New Algorithma and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321. https://doi.org/10.1093/sysbio/syq010
Guo X, Chen D (2010) Comparative evolution of the mitochondrial cytochrome b gene and nuclear S7 ribosomal protein gene intron 1 in sinipercid fishes and their relatives. Hydrobiologia 649(1):139–156. https://doi.org/10.1007/s10750-010-0236-5
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp 41:95–98
He SP, Mayden RL, Wang XZ, Wang W, Tang KL, Chen WJ, Chen YY (2008) Molecular phylogenetics of the family Cyprinidae (Actinopterygii: Cypriniformes) as evidenced by sequence variation in the first intron of S7 ribosomal protein-coding gene: further evidence from a nuclear gene of the systematic chaos in the family. Mol Phylogenet Evol 46:818–829
Hsu KC, Bor H, Lin HD, Kuo PH, Tan MS, Chiu YW (2014) Mitochondrial DNA phylogeography of Semisulcospira libertina (Gastropoda: Cerithioidea: Pleuroceridae): implications the history of landform changes in Taiwan. Mol Biol Rep 41(6):3733–3743. https://doi.org/10.1007/s11033-014-3238-y
Huang J (1945) Major division of tectonic units in China. Earthquake Press, Beijing, China (in Chinese)
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Monro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132. https://doi.org/10.1016/B978-1-4832-3211-9.50009-7
Kawamura K, Nagata Y, Ohtaka H, Kanoh Y, Kitamura J (2001) Genetic diversity in the Japanese rosy bitterling, Rhodeus ocellatus kurumeus (Cyprinidae). Ichthyol Res 48:369–378
Kottelat M (2001) Fishes of Laos. WHT publications ltd., Colombo 5, Sri Lanka, pp 198
Lang NJ, Mayden RL (2007) Systematics of the subgenus Oligocephalus (Teleostei: Percidae: Etheostoma) with complete subgeneric sampling of the genus Etheostoma. Mol Phylogenet Evol 43:605–615
Li S (1981) Studies on zoogeographical divisions for fresh water fishes of China. Science Press
Lin HD, Kuo PH, Wang WK, Chiu YW, Ju YM, Lin FJ, Hsu KC (2016) Speciation and differentiation of the genus Opsariichthys (Teleostei: Cyprinidae) in East Asia. Biochem Syst Ecol 68:92–100. https://doi.org/10.1016/j.bse.2016.07.001
Liu HZ (1998) A preliminary analysis to biogeographical process of the eastern Asian freshwater fishes. Acta Zootaxon Sin 23:49–55
Liu D, Guo HY, Tang WQ, Yang JQ (2012) Comparative evolution of S7 intron 1 and ribosomal internal transcribed spacer in Coilia nasus (Clupeiformes: Engraulidae). Int J Mol Sci 13(12):3085–3100. https://doi.org/10.3390/ijms13033085
Musilová Z, Rícan O, Janko K, Novák J (2008) Molecular phylogeny and biogeography of the neotropical cichlid fish tribe Cichlasomatini (Teleostei: Cichlidae: Cichlasomatinae). Mol Phylogenet Evol 46:659–672
Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105(1):207–217
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered vs. unordered alleles. Genetics 144(3):1237–1245
Qu Y, Zhang R, Quan Q, Song G, Li SH, Lei F (2012) Incomplete lineage sorting or secondary admixture: disentangling historical divergence from recent gene flow in the vinous-throated parrotbill (Paradoxornis webbianus). Mol Ecol 21(24):6117–6133. https://doi.org/10.1111/mec.12080
Rambaut A (2014) FigTree:1.3 Available at: http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Suchard MA, Xie D, Dremmond AJ (2014) Trace:v1.6 Available from http://tree.bio.ed.ac.uk/software/tracer/
Ren ME, Han TC (1959) The Jinsha River valley landforms and river-capture in northwestern Yunnan. Acta Geograph Sin 25:135–155
Rozas J, JC S-DB, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19(18):2496–2497. https://doi.org/10.1093/bioinformatics/btg359
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Templeton AR (1993) The “eve” hypotheses: a genetic critique and reanalysis. Am Anthropol 95(1):51–72. https://doi.org/10.1525/aa.1993.95.1.02a00030
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. https://doi.org/10.1093/nar/25.24.4876
Wang CF, Hsieh CH, Lee SC, Wang HY (2011) Systematics and phylogeography of the Taiwanese endemic minnow Candidia barbatus (Pisces: Cyprinidae) based on DNA sequence, allozymic, and morphological analyses. Zool J Linnean Soc 161(3):613–632. https://doi.org/10.1111/j.1096-3642.2010.00646.x
Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294:318
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 18:163–173
Yang S, Dong H, Lei F (2009) Phylogeography of regional fauna on the Tibetan plateau: a review. Prog Nat Sci 19:789–799
Yang JQ, Tang WQ, Liao TY, Sun Y, Zhou ZC, Han CC, Liu D, Lin HD (2012) Phylogeographical analysis on Squalidus argentatus recapitulates historical landscapes and drainage evolution on the island of Taiwan and mainland China. Int J Mol Sci 13(12):1405–1425. https://doi.org/10.3390/ijms13021405
Yang JQ, Hsu KC, Liu ZZ, Su LW, Kuo PH, Tang WQ, Lin HD (2016) The population history of Garra orientalis (Teleostei: Cyprinidae) using mitochondrial DNA and microsatellite data with approximate Bayesian computation. BMC Evol Biol 16(1):73. https://doi.org/10.1186/s12862-016-0645-9
Yap SY (2002) On the distributional patterns of southeast-east Asian freshwater fish and their history. J Biogeogr 29(9):1187–1199. https://doi.org/10.1046/j.1365-2699.2002.00771.x
Yu Y, Harris AJ, He X (2010) S-DIVA (statistical dispersal-Vicariance analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850
Zarza E, Reynoso VH, Emerson BC (2011) Discordant patterns of geographic variation between mitochondrial and microsatellite markers in the Mexican black iguana (Ctenosaura pectinata) in a contact zone. J Biogeogr 38(7):1394–1405. https://doi.org/10.1111/j.1365-2699.2011.02485.x
Zhang E (1999) Studies of morphometrics, systematic and biogeography of the cyprinid genus Sinilabeo, Rendahl 1932. PhD Thesis, Institute of Hydrobiology. Chinese Academy of Sciences
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 (in Chinese)
Zhang L, Tang QY, Liu HZ (2008) Phylogeny and speciated of eastern Asian cyprinid genus Sarcocheilichthys. J Fish Biol 72(5):1122–1137. https://doi.org/10.1111/j.1095-8649.2007.01733.x
Zheng HS (2004) Freshwater fish fauna and biogeography of eight rivers in East Guangdong, China. MSc dissertation, Institute of Zoology, South China Normal University, Guangzhou, China
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17(9):2107–2121. https://doi.org/10.1111/j.1365-294X.2008.03737.x
Acknowledgments
The research was supported by the National Natural Science Foundation of China (No. 31172066), and Shanghai Universities First-class Disciplines Project of Fisheries. This research supported by the Research Fund Program of Guangxi Key Lab of Mangrove Conservation and Utilization (Grant No. GKLMC-201307 and GKLMC-201404). We also thank the anonymous referees for their helpful comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics statement
The animal experiments were performed under an animal ethics approval granted by the Shanghai Ocean University. Our sampling procedures did not affect the survival of studies species.
Rights and permissions
About this article
Cite this article
Yang, JQ., Hsu, KC., Kuo, PH. et al. Mitochondrial and nuclear genetic structure in Rhodeus ocellatus (Teleostei: Cyprinidae) with approximate Bayesian computation. Environ Biol Fish 101, 829–841 (2018). https://doi.org/10.1007/s10641-018-0741-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-018-0741-3