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Genetic analysis of population differentiation and adaptation in Leuciscus waleckii

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Abstract

Demographic events and natural selection both influence animal phenotypic and genetic variation; exploring the effects of demography and selection on population divergence is of great significance in evolutionary biology. To uncover the causes behind the patterns of genetic differentiation and adaptation among six populations of Leuciscus waleckii from Dali Basin (two populations, alkaline vs. freshwater) and Amur Basin (four populations, freshwater rivers vs. alkaline lake), a set of 21 unlinked polymorphic microsatellite markers and two mitochondrial DNA sequences (Cytb and D-loop) were applied to examine whether populations from different environments or habitats have distinct genetic differentiation and whether alkalinity is the major factor that caused population divergence. Bayesian analysis and principal component analysis as well as haplotype network analysis showed that these populations are primarily divided into two groups, which are congruent with geographic separation but not inconsistent with the habitat environment (alkalinity). Using three different approaches, outlier detection indicated that one locus, HLJYL017, may be under directional selection and involved in local adaptation processes. Overall, this study suggested that demographic events and selection of local environmental conditions including of alkalinity are jointly responsible for population divergence. These findings constitute an important step towards the understanding of the genetic basis of differentiation and adaptation, as well as towards the conservation of L. waleckii.

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References

  • Allendorf FW, Bayles D, Bottom DL, Currens KP, Frissell CA, Hankin D, Lichatowich JA, Nehlsen W, Trotter PC, Williams TH (1997) Prioritizing Pacific salmon stocks for conservation. Conserv Biol 11:140–152

    Article  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323. doi:10.1186/1471-2105-9-323

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  Google Scholar 

  • Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980. doi:10.1111/j.1365-294X.2004.02125.x

    Article  CAS  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626. doi:10.1098/rspb.1996.0237

    Article  Google Scholar 

  • Bradic M, Beerli P, García-de León FJ, Esquivel-Bobadilla S, Borowsky RL (2012) Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus). BMC Evol Biol 12:9. doi:10.1186/1471-2148-12-9

    Article  Google Scholar 

  • Cano JM, Shikano T, Kuparinen A, Merila J (2008) Genetic differentiation, effective population size and gene flow in marine fishes: implications for stock management. J Integr Field Sci 5:1–10

    Google Scholar 

  • Chang YM, Liang LQ, Ma HT, He JG, Sun XW (2008) Microsatellite analysis of genetic diversity and population structure of Chinese mitten crab (Eriocheir sinensis). J Genet Genomics 35:171–176. doi:10.1111/j.1365-294X.2006.03133.x

    Article  CAS  Google Scholar 

  • Chi BJ (2010) Genetic variability of Leuciscus waleckii (Dybowski) and construction of the cDNA substractive library of saline-alkaline tolerance. Shanghai Ocean University, Master Dissertation

    Google Scholar 

  • Chi BJ, Chang YM, Yan XC, Cao DJ, Li Y, Gao YK, Liu YH, Liang LQ (2010) Genetic variability and genetic structure of Leuciscus waleckii Dybowski in Wusuli River and Dali Lake. J Fish Sci China 17:228–235

    CAS  Google Scholar 

  • Collin H, Fumagalli L (2011) Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae). Mol Ecol 20:4490–4502. doi:10.1111/j.1365-294X.2011.05284.x

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  Google Scholar 

  • Coscia I, Vogiatzi E, Kotoulas G, Tsigenopoulos C, Mariani S (2011) Exploring neutral and adaptive processes in expanding populations of gilthead sea bream, Sparus aurata L., in the North-East Atlantic. Heredity 108:537–546. doi:10.1038/hdy.2011.120

    Article  Google Scholar 

  • Egan SP, Nosil P, Funk DJ (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62:1162–1181. doi:10.1111/j.1558-5646.2008.00352.x

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  Google Scholar 

  • 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 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298. doi:10.1038/hdy.2009.74

    Article  CAS  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752. doi:10.1046/j.0962-1083.2001.01411.x

    CAS  Google Scholar 

  • Geng K, Zhang ZC (1988) The geomorphic characteristics and evolution of the lakes in Dalairuoer area of Neimenggu Plateau during the Holocene. J Beijing Normal Univ (Nat Sci) 4:94–101

    Google Scholar 

  • Gienapp P, Teplitsky C, Alho J, Mills J, Merilä J (2007) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178. doi:10.1111/j.1365-294X.2007.03413.x

    Article  Google Scholar 

  • Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015. doi:10.1046/j.1365-294X.2002.01495.x

    Article  CAS  Google Scholar 

  • Hendry AP, Taylor EB (2004) How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 58:2319–2331. doi:10.1111/j.0014-3820.2004.tb01606.x

    Google Scholar 

  • Hu WG, Duan ZY, Wang JF, Sheng JL, Ma RL (2004) Divergence and systematical evolution of three Leuciscus species in Xinjiang based on mitochondrial DNA control region sequences. J Genet Genomics 31:970–975

    CAS  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  • Kim Y, Stephan W (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765–777

    CAS  Google Scholar 

  • Li SZ (1981) Distribution division of Chinese freshwater fishes. Science Press, Beijing

    Google Scholar 

  • Li ZM, Liu HT, Feng WY, Du ZH, Meng HP, Zhang L, Liu CR, Hu GX (2008) Comparative studies on four isoenzymes of Leuciscus waleckii and Carassius auratus in Dali Lake and Ganggeng Lake. Freshw Fish 38:26–29

    CAS  Google Scholar 

  • Liu JL (2011) Isolation of microsatellite markers from genome of Leuciscus waleckii and analysis of genetic diversity in five Leuciscus populations. Master Dissertation, Shanghai Ocean University

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129. doi:10.1093/bioinformatics/bti282

    Article  CAS  Google Scholar 

  • Liu JL, Chang YM, Xu LH, Liu CL, Liang LQ, Han GC, Gao YK, Liu YH (2011) Isolation and characterization of microsatellite from genome of Leuciscus waleckii Dybowski. Acta Agriculturae Boreali-Sinica 26:87–93

    Google Scholar 

  • Luikart G, Allendorf F, Cornuet J, Sherwin W (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247. doi:10.1093/jhered/89.3.238

    Article  CAS  Google Scholar 

  • Ma B, Lui T, Zhang Y, Chen J (2012) Phylogeography and population genetic structure of Amur Grayling Thymallus grubii in the Amur Basin. Asian-Aust J Anim Sci 25:935–944

    Article  Google Scholar 

  • Mohammadi S, Prasanna B (2003) Analysis of genetic diversity in crop plants—salient statistical tools and considerations. Crop Sci 43:1235–1248. doi:10.2135/cropsci2003.1235

    Article  Google Scholar 

  • Nielsen EE, Hansen MM, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol Ecol 15:3219–3229. doi:10.1111/j.1365-294X.2006.03025.x

    Article  CAS  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150. doi:10.1111/j.1365-294X.2009.04272.x

    Article  Google Scholar 

  • Nosil P (2008) Speciation with gene flow could be common. Mol Ecol 17:2103–2106. doi:10.1111/j.1365-294X.2008.03715.x

    Article  Google Scholar 

  • Paris M, Boyer S, Bonin A, Collado A, David JP, Despres L (2010) Genome scan in the mosquito Aedes rusticus: population structure and detection of positive selection after insecticide treatment. Mol Ecol 19:325–337. doi:10.1111/j.1365-294X.2009.04437.x

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Pyhäjärvi T, García-Gil MR, Knürr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177:1713–1724

    Article  Google Scholar 

  • Qi DL (2009) Genetic variation and diversity of Gymncypris eckloni in the upper Yellow River inferred from mitochondrial cytochrome b gene. Zool Res 3:255–261

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rohlf FJ (2000) Statistical power comparisons among alternative morphometric methods. Am J Phys Anthropol 111:463–478. doi:10.1002/(SICI)1096-8644(200004)111:4<463:AID-AJPA3>3.0.CO;2-B

    Article  CAS  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    Article  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359

    Article  CAS  Google Scholar 

  • Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi:10.1111/j.1461-0248.2004.00715.x

    Article  Google Scholar 

  • Saint-Laurent R, Legault M, Bernatchez L (2003) Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Mol Ecol 12:315–330. doi:10.1046/j.1365-294X.2003.01735.x

    Article  CAS  Google Scholar 

  • Schlötterer C (2003) Hitchhiking mapping–functional genomics from the population genetics perspective. Trends Genet 19:32–38

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New York

    Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–793. doi:10.1126/science.3576198

    Article  CAS  Google Scholar 

  • Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688. doi:10.1111/j.1365-294X.2005.02437.x

    Article  CAS  Google Scholar 

  • Suk H, Neff B (2009) Microsatellite genetic differentiation among populations of the Trinidadian guppy. Heredity 102:425–434. doi:10.1038/hdy.2009.7

    Article  CAS  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. doi:10.1093/bioinformatics/btn478

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wilis DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Vasemägi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22:1067–1076. doi:10.1093/molbev/msi093

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569. doi:10.1098/rspb.2005.3356

    Article  Google Scholar 

  • Wang J, Feng WY, Zhang L, Zong ZD, Meng HP, Peng BC, Li ZL (2011) Monitoring and evaluation on water quality and biology resource quantity in Hulun Lake. J Hydroecol 32:64–68

    Google Scholar 

  • Willing E, Bentzen P, van Oosterhout C, Hoffmann M, Cable J, Breden F, Weigel D, Dreyer C (2010) Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Mol Ecol 19:968–984. doi:10.1111/j.1365-294X.2010.04528.x

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    Google Scholar 

  • Wong B, Keogh J, McGlashan D (2004) Current and historical patterns of drainage connectivity in eastern Australia inferred from population genetic structuring in a widespread freshwater fish Pseudomugil signifer (Pseudomugilidae). Mol Ecol 13:391–401. doi:10.1046/j.1365-294X.2003.02085.x

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the National High-tech Research and Development Program of China (2011AA100402-3).

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Authors and Affiliations

  1. Heilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Rd 232 Hesong, Daoli District, Harbin, 150070, China

    Yumei Chang, Ran Tang, Xiaowen Sun & Liqun Liang

  2. Guangdong Entomological Institute/South China Institute of Endangered Animals, Guangzhou, 510260, China

    Jinping Chen

  3. Fisheries and Life Science College, Shanghai Ocean University, Shanghai, 201306, China

    Jinfeng Huang & Xinjie Dou

  4. School of Marine Science, Ningbo University, Ningbo, 315211, China

    Ran Tao

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  1. Yumei Chang
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  2. Ran Tang
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Chang, Y., Tang, R., Sun, X. et al. Genetic analysis of population differentiation and adaptation in Leuciscus waleckii . Genetica 141, 417–429 (2013). https://doi.org/10.1007/s10709-013-9741-6

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