期刊论文详细信息
BMC Evolutionary Biology
Genetic variation in brown trout Salmo trutta across the Danube, Rhine, and Elbe headwaters: a failure of the phylogeographic paradigm?
Steven Weiss2  Theodora Kopun1  Ulrich Schliewen3  Estelle Lerceteau-Köhler4 
[1] Institute of Plant Sciences, Karl-Franzens University Graz, Schubertstraße 51, A-8010 Graz Austria;Institute of Zoology, Karl-Franzens University Graz, Universitätsplatz 2, A-8010 Graz Austria;Department of Ichthyology, Bavarian State Collection of Zoology (ZSM), Münchhausenstr. 21, D-81247, München Germany;Department of Plant Biology and Forest Genetics,Uppsala BioCenter, Swedish University of Agricultural Sciences (SLU), Box 7080, S-750 07 Uppsala Sweden
关键词: Conservation;    Stocking;    LDH-C1;    Microsatellites;    mtDNA;    Bavaria;    Austria;    Alpine;    Phylogeography;    Paleo-hydrology;   
Others  :  1086550
DOI  :  10.1186/1471-2148-13-176
 received in 2013-03-06, accepted in 2013-08-15,  发布年份 2013
PDF
【 摘 要 】

Background

Brown trout Salmo trutta have been described in terms of five major mtDNA lineages, four of which correspond to major ocean basins, and one, according to some authors, to a distinct taxon, marbled trout Salmo marmoratus. The Atlantic and Danubian lineages of brown trout meet in a poorly documented contact zone in Central Europe. The natural versus human mediated origin of the Atlantic lineage in the upper Danube is a question of both theoretical and practical importance with respect to conservation management. We provide a comprehensive population genetic analysis of brown trout in the region with the aim of evaluating the geographic distribution and genetic integrity of these two lineages in and around their contact zone.

Results

Genetic screening of 114 populations of brown trout across the Danube/Rhine/Elbe catchments revealed a counter-intuitive phylogeographic structure with near fixation of the Atlantic lineage in the sampled portions of the Bavarian Danube. Along the Austrian Danube, phylogeographic informative markers revealed increasing percentages of Danube-specific alleles with downstream distance. Pure Danube lineage populations were restricted to peri-alpine isolates within previously glaciated regions. Both empirical data and simulated hybrid comparisons support that trout in non-glaciated regions north and northeast of the Alps have an admixed origin largely based on natural colonization. In contrast, the presence of Atlantic basin alleles south and southeast of the Alps stems from hatchery introductions and subsequent introgression. Despite extensive stocking of the Atlantic lineage, little evidence of first generation stocked fish or F1 hybrids were found implying that admixture has been established over time.

Conclusions

A purely phylogeographic paradigm fails to describe the distribution of genetic lineages of Salmo in Central Europe. The distribution pattern of the Atlantic and Danube lineages is extremely difficult to explain without invoking very strong biological mechanisms.

The peri-alpine distribution of relict populations of pure Danubian lineage brown trout implies that they colonized headwater river courses post-glacially ahead of the expansion of the Atlantic lineage. The recognition of natural as opposed to anthropogenic introgression of the Atlantic lineage into Danubian gene pools is of fundamental importance to management strategies.

【 授权许可】

   
2013 Lerceteau-Köhler et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150116012827512.pdf 2104KB PDF download
Figure 7. 58KB Image download
20151107030206349.pdf 486KB PDF download
Figure 5. 24KB Image download
Figure 4. 38KB Image download
Figure 3. 36KB Image download
Figure 2. 55KB Image download
Figure 1. 92KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 7.

【 参考文献 】
  • [1]Avise JC: Twenty-five key evolutionary insights from the phylogeographic revolution in population genetics. In Phylogeography of southern european refugia. Edited by Weiss S, Ferrand N. Dordrecht, The Netherlands: Springer; 2006:7-21.
  • [2]Moritz C, McGuigan K, Bernatchez L: Conservation of freshwater fishes: integrating evolution and genetics with ecology. In Freshwater Fish Conservation: options for the future. Edited by Collares-Pereira MJ, Coelho MM, Cowx IG. Oxford: Blackwell Science; 2002:293-310.
  • [3]Salzburger W, Brandstatter A, Gilles A, Parson W, Hempel M, Sturmbauer C, Meyer A: Phylogeography of the vairone (Leuciscus souffia, Risso 1826) in Central Europe. Mol Ecol 2003, 12(9):2371-2386.
  • [4]Gross R, Kühn R, Baars M, Schröder W, Stein H, Rottmann O: Genetic differentiation of European grayling populations across the Main, Danube and Elbe drainages in Bavaria. J Fish Biol 2001, 58(1):264-280.
  • [5]Englbrecht CC, Freyhof J, Nolte A, Rassmann K, Schliewen U, Tautz D: Phylogeography of the bullhead Cottus gobio (Pisces: Teleostei: Cottidae) suggests a pre-pleistocene origin of the major central European populations. Mol Ecol 2000, 9(6):709-722.
  • [6]Nesbo CL, Fossheim T, Vollestad LA, Jakobsen KS: Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol Ecol 1999, 8(9):1387-1404.
  • [7]Durand JD, Persat H, Bouvet Y: Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol Ecol 1999, 8(6):989-997.
  • [8]Konopinski MK, Amirowicz A, Kukula K: Probable direction of the postglacial colonization of rivers on northern slopes of the Carpathian Ridge by Barbus carpathicus (Teleostei: Cyprinidae) evidenced by cline of genetic variation. J Fish Biol 2007, 70:406-415.
  • [9]Bânârescu P: Zoogeography of fresh waters, Volume 2: distribution and dispersal of freshwater animals in North America and Eurasia. Wiesbaden: AULA-Verlag; 1991.
  • [10]Allendorf F, Ryman N, Stennek A, Stahl G: Genetic-variation in Scandinavian brown trout (Salmo trutta L) - evidence of distinct sympatric populations. Hereditas 1976, 83(1):73-82.
  • [11]Ryman N, Allendorf FW, Stahl G: Reproductive isolation with little genetic divergence in sympatric populations of brown trout (Salmo trutta). Genetics 1979, 92(1):247-262.
  • [12]Ferguson A, Mason FM: Allozyme evidence for reproductively isolated sympatric populations of brown trout Salmo trutta L in Lough Melvin, Ireland. J Fish Biol 1981, 18(6):629-642.
  • [13]Bernatchez L, Guyomard R, Bonhomme F: DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Mol Ecol 1992, 1(3):161-173.
  • [14]Bernatchez L: The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 2001, 55(2):351-379.
  • [15]Cortey M, Pla C, Garcia-Marin JL: Historical biogeography of Mediterranean trout. Mol Phylogenet Evol 2004, 33(3):831-844.
  • [16]Sušnik S, Snoj A, Wilson IF, Mrdak D, Weiss S: Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative. Mol Phylogenet Evol 2007, 44(1):63-76.
  • [17]Apostolidis AP, Madeira MJ, Hansen MM, Machordom A: Genetic structure and demographic history of brown trout (Salmo trutta) populations from the southern Balkans. Freshwater Biol 2008, 53(8):1555-1566.
  • [18]Suárez J, Bautista JM, Almodóvar A, Machordom A: Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 2001, 87:198-206.
  • [19]Martinez P, Bouza C, Castro J, Hermida M, Pardo BG, Sanchez L: Analysis of a secondary contact between divergent lineages of brown trout Salmo trutta L. from Duero basin using microsatellites and mtDNA RFLPs. J Fish Bio 2007, 71B:195-213.
  • [20]Snoj A, Maric S, Bajec SS, Berrebi P, Janjani S, Schoffmann J: Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Mol Phylogenet Evol 2011, 61(1):203-211.
  • [21]Splendiani A, Giovannotti M, Cerioni PN, Caniglia ML, Caputo V: Phylogeographic inferences on the native brown trout mtDNA variation in central Italy. Ital J Zool 2006, 73(2):179-189.
  • [22]Apostolidis AP, Triantaphyllidis C, Kouvatsi A, Economidis PS: Mitochondrial DNA sequence variation and phylogeography among Salmo trutta L (Greek brown trout) populations. Mol Ecol 1997, 6(6):531-542.
  • [23]Sušnik S, Schoffmann J, Weiss S: Genetic verification of native brown trout from the Persian Gulf (Catak Cay River, Tigris basin). J Fish Biol 2005, 67(3):879-884.
  • [24]Kottelat M, Freyhof J: Handbook of European Freshwater Fishes. Cornol: Kottelat, Berlin: Freyhof; 2007.
  • [25]Weiss S, Schlotterer C, Waidbacher H, Jungwirth M: Haplotype (mtDNA) diversity of brown trout Salmo trutta in tributaries of the Austrian Danube: massive introgression of Atlantic basin fish - by man or nature? Mol Ecol 2001, 10(5):1241-1246.
  • [26]Riffel M, Storch V, Schreiber A: Allozyme variability of brown trout (Salmo trutta L.) populations across the Rhenanian-Danubian watershed in southwest Germany. Heredity 1995, 74(3):241-249.
  • [27]Weiss S, Antunes A, Schlotterer C, Alexandrino P: Mitochondrial haplotype diversity among Portuguese brown trout Salmo trutta L. populations: relevance to the post-Pleistocene recolonization of northern Europe. Mol Ecol 2000, 9(6):691-698.
  • [28]Hantke R: Flußgeschichte Mitteleuropas – Skizzen zu einer, Vegetations- und Klimageschichte der letzten 40 Millionen Jahre. Stuttgart: Ferdinand Enke Verlag; 1993.
  • [29]Schliewen U, Englbrecht C, Rassmann K, Miller M, Klein L, Tautz D: Veränderungen der genetischen Vielfalt: Molekulare und populations-ökologische Charkterisierung autochoner und durch Besatz beeinflusster Salmoniden-Populationen (Bachforelle, Alpen-Seesaibling) in Bayern. Berlin: Umweltbundesamt; 2001:206. Available through http://www.umweltdaten.de/publikationen/fpdf-l/2014.pdf webcite
  • [30]Baric S, Riedl A, Meraner A, Medgyesy N, Lackner R, Pelster B, Via JD: Alpine headwater streams as reservoirs of remnant populations of the Danubian clade of brown trout. Freshwater Biol 2010, 55(4):866-880.
  • [31]van Husen D: Die Ostalpen in den Eiszeiten: palägeographischen Karte der letzen Eiszeit 1:5000.000. Wien: Geologische Bundesanstallt; 1987.
  • [32]Kohout J, Jaškova I, Papoušek I, Šedivá A, Šlechta V: Effects of stocking on the genetic structure of brown trout, Salmo trutta, in Central Europe inferred from mitochondrial and nuclear DNA markers. Fisheries Manag Ecol 2012, 19:252-263.
  • [33]Winkler KA, Pamminger-Lahnsteiner B, Wanzenbock J, Weiss S: Hybridization and restricted gene flow between native and introduced stocks of Alpine whitefish (Coregonus sp.) across multiple environments. Mol Ecol 2011, 20(3):456-472.
  • [34]Fink J: Die Paläogeographie der Donau. In Limnologie der Donau. vol. Teil III. Stuttgart: Schweizerbar’scher Verlagsbuchhandlung; 1966:1-50.
  • [35]Ibetsberger H, Jäger P, Häupl M: Der Zerfall des Salzachgletschers und die nacheiszeitliche Entwicklung des Salzburger Gewässersystems aus der Sicht der Wiederbesiedlung der Salzburger Gewässer mit Fischen. In Nacheiszeitliche Entwicklung des Salzburger Gewässernetzes. Land Salzburg: Österreich; 2010:7-54.
  • [36]Meier K, Hansen MM, Bekkevold D, Skaala O, Mensberg KLD: An assessment of the spatial scale of local adaptation in brown trout (Salmo trutta L.): footprints of selection at microsatellite DNA loci. Heredity 2011, 106(3):488-499.
  • [37]Keller I, Taverna A, Seehausen O: Evidence of neutral and adaptive genetic divergence between European trout populations sampled along altitudinal gradients. Mol Ecol 2011, 20(9):1888-1904.
  • [38]Weiss S, Kopun T, Sušnik Bajec S: Assessing natural and disturbed population structure in European grayling, Thymallus thymallus (Salmonidae): melding phylogeographic, population genetic, and jurisdictional perspectives for conservation planning. J Fish Biol 2013, 82(2):505-521.
  • [39]Miller SA, Dykes DD, Polesky HF: A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988, 16(3):1215-1215.
  • [40]Lerceteau-Köhler E, Weiss S: Development of a multiplex PCR microsatellite assay in brown trout Salmo trutta, and its potential application for the genus. Aquaculture 2006, 258(1–4):641-645.
  • [41]Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4(3):535-538.
  • [42]McMeel OM, Hoey EM, Ferguson A: Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1*90 and*100 alleles. Mol Ecol 2001, 10(1):29-34.
  • [43]Hamilton KE, Ferguson A, Taggart JB, Tomasson T, Walker A, Fahy E: Post-glacial colonization of brown trout, Salmo trutta L - LDH-5 as a phylogeographic marker locus. J Fish Biol 1989, 35(5):651-664.
  • [44]Goudet J: FSTAT, version 2.9.3: a program to estimate and test gene diversities and fixation indices. [Available via http://www2.unil.ch/popgen/softwares/fstat.htm webcite]
  • [45]Excoffier L, Smouse PE, Quattro JM: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131(2):479-491.
  • [46]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 2005, 1:47-50.
  • [47]Hardy OJ, Charbonnel N, Freville H, Heuertz M: Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 2003, 163(4):1467-1482.
  • [48]Hardy OJ, Vekemans X: SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2(4):618-620.
  • [49]Goudet J: PCAGEN 1.2. [Available via http://www2.unil.ch/popgen/softwares/pcagen.htm webcite]
  • [50]Langella O: Populations 1.2.30. [Available http://bioinformatics.org/~tryphon/populations webcite]
  • [51]Cavalli-Sforza LL, Edwards AWF: Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 1967, 19:233-257.
  • [52]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155(2):945-959.
  • [53]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14(8):2611-2620.
  • [54]Peakall R, Smouse PE: GenAlEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 2006, 6(1):288-295.
  • [55]Reich DE, Goldstein DB: Genetic evidence for a paleolithic human population expansion in Africa (vol 95, pg 8119, 1998). Proc Natl Acad Sci U S A 1998, 95(18):11026-11026.
  • [56]Bilgin R: Kgtests: a simple excel macro program to detect signatures of population expansion using microsatellites. Mol Ecol Notes 2007, 7(3):416-417.
  • [57]Reich DE, Feldman MW, Goldstein DB: Statistical properties of two tests that use multilocus data sets to detect population expansions. Mol Biol Evol 1999, 16(4):453-466.
  • [58]Anderson EC, Thompson EA: A model-based method for identifying species hybrids using multilocus genetic data. Genetics 2002, 160(3):1217-1229.
  文献评价指标  
  下载次数:86次 浏览次数:48次