Conservation Genetics

, Volume 14, Issue 4, pp 809–821

Microsatellite markers reveal clear geographic structuring among threatened noble crayfish (Astacus astacus) populations in Northern and Central Europe

  • Riho Gross
  • Stefan Palm
  • Kuldar Kõiv
  • Tore Prestegaard
  • Japo Jussila
  • Tiit Paaver
  • Juergen Geist
  • Harri Kokko
  • Anna Karjalainen
  • Lennart Edsman
Research Article

Abstract

Noble crayfish (Astacus astacus L.), the most highly valued freshwater crayfish in Europe, is threatened due to a long-term population decline caused mainly by the spread of crayfish plague. Reintroduction of the noble crayfish into restored waters is a common practice but the geographic and genetic origin of stocking material has rarely been considered, partially because previous genetic studies have been hampered by lack of nuclear gene markers with known inheritance. This study represents the first large scale population genetic survey of the noble crayfish (633 adults from 18 locations) based on 10 newly developed microsatellite markers. We focused primarily on the Baltic Sea area (Estonia, Finland and Sweden) where the largest proportion of the remaining populations exists. To allow comparisons, samples from the Black Sea catchment (the Danube drainage) were also included. Two highly differentiated population groups were identified corresponding to the Baltic Sea and the Black Sea catchments, respectively. The Baltic Sea catchment populations had significantly lower genetic variation and private allele numbers than the Black Sea catchment populations. Within the Baltic Sea area, a clear genetic structure was revealed with population samples corresponding well to their geographic origin, suggesting little impact of long-distance translocations. The clear genetic structure strongly suggests that the choice of stocking material for re-introductions and supplemental releases needs to be based on empirical genetic knowledge.

Keywords

Genetic variation Genetic differentiation Population structure Microsatellite DNA Conservation genetics 

References

  1. Agerberg A (1990) Genetic variation in three species of freshwater crayfish; Astacus astacus L., Astacus leptodactylus Aesch., and Pacifastacus leniusculus (Dana), revealed by isozyme electrophoresis. Hereditas 113:101–108CrossRefGoogle Scholar
  2. Alaranta A, Henttonen P, Jussila J, Kokko H, Prestegaard T, Edsman L, Halmekytö M (2006) Genetic differences among noble crayfish (Astacus astacus) stocks in Finland, Sweden and Estonia based on the ITS1 region. Bull Fr Pêche Piscic 380–381:965–976CrossRefGoogle Scholar
  3. Alaranta A, Jussila J, Kokko H (2011) Inheritance of ITS1 region microsatellite-like repeats in the noble crayfish, Astacus astacus (Decapoda, Astacidea). Crustaceana 84:1325–1336CrossRefGoogle Scholar
  4. Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337PubMedCrossRefGoogle Scholar
  5. Alm G (1929) Der Krebs und die Krebspest in Schweden. Zeitschrift für Fisherei 27:123–138 (in German)Google Scholar
  6. Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–451CrossRefGoogle Scholar
  7. Bohman P, Nordwall F, Edsman L (2006) The effect of the large-scale introduction of signal crayfish on the spread of crayfish plague in Sweden. Bull Fr Pêche Piscic 380–381:1291–1302CrossRefGoogle Scholar
  8. Diéguez-Uribeondo J, Cerenius L, Dyková I, Gelder S, Henntonen P, Jiravanichpaisal P, Lom J, Söderhäll K (2006) Pathogens, parasites and ectocommensals. In: Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (eds) Atlas of Crayfish in Europe, Patrimoines naturels, 64. Muséum national d’Histoire naturelle, Paris, pp 133–149Google Scholar
  9. Edsman L (2004) The Swedish story about import of live crayfish. Bull Fr Pêche Piscic 372–373:281–288CrossRefGoogle Scholar
  10. Edsman L, Schröder S (2009) Action plan for noble crayfish 2008–2013 (Astacus astacus). Fiskeriverket och Naturvårdsverket, Rapport 5955 (In Swedish with English summary)Google Scholar
  11. Edsman L, Farris JS, Källersjö M, Prestegaard T (2002) Genetic differentiation between noble crayfish, Astacus astacus (L.), populations detected by microsatellite length variation in the rDNA ITS1 region. Bull Fr Pêche Piscic 36:691–706CrossRefGoogle Scholar
  12. Edsman L, Füreder L, Gherardi F, Souty-Grosset C (2010) Astacus astacus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. http://www.iucnredlist.org/details/2191/0. Accessed 08 February 2013
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  14. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  15. Farkac J, Král D, Škorpík M (eds) (2005) List of threatened species in the Czech Republic. Invertebrates, Agentura ochrany prírody a krajiny CR, PrahaGoogle Scholar
  16. Fevolden SE, Taugbøl T, Skurdal J (1994) Allozymic variation among populations of noble crayfish, Astacus astacus L., in southern Norway: implications for management. Aquac Res 25:927–935CrossRefGoogle Scholar
  17. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005) Candidate genes for behavioural ecology. Trends Ecol Evol 20:96–104PubMedCrossRefGoogle Scholar
  18. Füreder L, Edsman L, Holdich DM, Kozák P, Machino Y, Pöckl M, Renai B, Reynolds J, Schulz H, Sint D, Taugbøl T, Trouilhé MC (2006) Indigenous crayfish habitat and threats. In: Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (eds) Atlas of Crayfish in Europe, Patrimoines naturels, 64. Muséum national d’Histoire naturelle, Paris, pp 25–48Google Scholar
  19. Gärdenfors U (ed) (2010) The 2010 Red List of Swedish Species. ArtDatabanken, SLU, Uppsala. http://www.artfakta.se/GetSpecies.aspx?SearchType=Advanced. Accessed 20 February 2013
  20. Geist J (2011) Integrative freshwater ecology and biodiversity conservation. Ecol Ind 11:1507–1516CrossRefGoogle Scholar
  21. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 27 September 2012
  22. Gouin N, Grandjean F, Bouchon D, Reynolds JD, Souty-Grosset C (2001) Population genetic structure of the endangered freshwater crayfish Austropotamobius pallipes, assessed using RAPD markers. Heredity 87:80–87PubMedCrossRefGoogle Scholar
  23. Gouin N, Grandjean F, Souty-Grosset C (2006) Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications. Freshwater Biol 51:1369–1387CrossRefGoogle Scholar
  24. Grandjean F, Souty-Grosset C (2000) Mitochondrial DNA variation and population genetic structure of the white-clawed crayfish, Austropotamobius pallipes pallipes. Cons Genet 1:309–319CrossRefGoogle Scholar
  25. Gren IM, Campos M, Edsman L, Bohman P (2009) Incomes, attitudes, and occurrences of invasive species: an application to signal crayfish in Sweden. Environ Manage 43:210–220PubMedCrossRefGoogle Scholar
  26. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  27. Gydemo R, Gydemo R (1990). Utsättningar av flodkräfta i Västerbottens län. Rapport Swedish University of Agricultural Sciences, Department of Aquaculture, 4 (In Swedish)Google Scholar
  28. Hansen MM, Meier K, Mensberg K-LD (2010) Identifying footprints of selection in stocked brown trout populations: a spatio-temporal approach. Mol Ecol 19:1787–1800PubMedCrossRefGoogle Scholar
  29. Harris DJ, Crandall KA (2000) Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Mol Biol Evol 17:284–291PubMedCrossRefGoogle Scholar
  30. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99:592–600PubMedCrossRefGoogle Scholar
  31. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112CrossRefGoogle Scholar
  32. Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manage Aquat Ecosyst 394–395:11CrossRefGoogle Scholar
  33. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  34. Jeukens J, Bernatchez L (2012) Regulatory versus coding signatures of natural selection in a candidate gene involved in the adaptive divergence of whitefish species pairs (Coregonus spp.). Ecol Evol 2:258–271PubMedCrossRefGoogle Scholar
  35. Jussila J, Mannonen A (2004) Crayfisheries in Finland, a short overview. Bull Fr Pêche Piscic 372–373:263–274CrossRefGoogle Scholar
  36. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  37. Kõiv K, Gross R, Paaver T, Kuehn R (2008) Isolation and characterization of first microsatellite markers for the noble crayfish, Astacus astacus. Cons Genet 9:1703–1706CrossRefGoogle Scholar
  38. Kõiv K, Gross R, Paaver T, Hurt M, Kuehn R (2009) Isolation and characterization of 11 novel microsatellite DNA markers in the noble crayfish, Astacus astacus. Anim Genet 40:124–126PubMedCrossRefGoogle Scholar
  39. Koskinen MT, Nilsson J, Veselov AJe, Potutkin AG, Ranta E, Primmer CR (2002) Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae. Heredity 88:391–401PubMedCrossRefGoogle Scholar
  40. Laikre L, Ryman N (1996) Effects on intraspecific biodiversity from harvesting and enhancing natural populations. Ambio 25:504–509Google Scholar
  41. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19:4293PubMedCrossRefGoogle Scholar
  42. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170PubMedCrossRefGoogle Scholar
  43. Nesbø CL, Fossheim T, Vøllestad A, Jakobsen KS (1999) Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol Ecol 8:1387–1404PubMedCrossRefGoogle Scholar
  44. Nilsson J, Gross R, Asplund T, Dove O, Jansson H, Kelloniemi J, Kohlmann K, Löytynoja A, Nielsen EE, Paaver T, Primmer CR, Titov S, Vasemägi A, Veselov A, Öst T, Lumme J (2001) Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol Ecol 10:89–102PubMedCrossRefGoogle Scholar
  45. Ota T (1993) DISPAN: Genetic Distance and Phylogenetic Analysis Software. Pennsylvania State University, USA. http://iubio.bio.indiana.edu/soft/molbio/ibmpc/dispan.zip. Accessed 27 September 2012
  46. Oug E, Brattegard T, Vader W, Christiansen ME, Walseng B, Djursvoll P (2010) Krepsdyr (Crustacea). In: Kålås JA, Viken Å, Henriksen S, Skjelseth S (eds) The 2010 Norwegian Red List for Species. Norwegian Biodiversity Information Centre, Norway, pp 209–221Google Scholar
  47. Paaver T, Hurt M (2009) Status and management of noble crayfish Astacus astacus in Estonia. Knowl Manage Aquat Ecosyst 344–345:42–45Google Scholar
  48. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  49. Raymond M, Rousset F (1995a) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  50. Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  51. Reynolds J, Souty-Grosset C (2012) Management of freshwater biodiversity: crayfish as bioindicators. Cambridge University Press, New YorkGoogle Scholar
  52. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  53. Säisä M, Koljonen M-L, Gross R, Nilsson J, Tähtinen J, Koskiniemi J, Vasemägi A (2005) Population genetic structure and postglacial colonization of Atlantic salmon (Salmo salar) in the Baltic Sea area based on microsatellite DNA variation. Can J Fish Aquat Sci 62:1887–1904CrossRefGoogle Scholar
  54. Säisä M, Salminen M, Koljonen M-L, Ruuhijärvi J (2010) Coastal and freshwater pikeperch (Sander lucioperca) populations differ genetically in the Baltic Sea basin. Hereditas 147:205–214PubMedCrossRefGoogle Scholar
  55. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  56. Santucci F, Iaconelli M, Andreani P, Cianchi R, Nascetti G, Bullini L (1997) Allozyme diversity of European freshwater crayfish of the genus Austropotamobius. Bull Fr Pêche Piscic 347:663–676CrossRefGoogle Scholar
  57. Schrimpf A, Schulz HK, Theissinger K, Pârvulescu L, Schulz R (2011) The first large-scale genetic analysis of the vulnerable noble crayfish Astacus astacus reveals low haplotype diversity in central European populations. Knowl Manage Aquat Ecosyst 401:35p1–35p14Google Scholar
  58. Schulz R (2000) Status of the noble crayfish Astacus astacus (L.) in Germany: monitoring protocol and the use of RAPD markers to assess the genetic structure of populations. Bull Fr Pêche Piscic 356:123–138CrossRefGoogle Scholar
  59. Schulz HK, Śmietana P, Schulz R (2004) Assessment of DNA variations of the noble crayfish (Astacus astacus L.) in Germany and Poland using inter-simple sequence repeats (ISSRS). Bull Fr Pêche Piscic 372–373:387–399CrossRefGoogle Scholar
  60. Skurdal J, Taugbøl T, Burba A, Edsman L, Söderbäck B, Styrishave B, Tuusti J, Westman K (1999) Crayfish introductions in the Nordic and Baltic countries. In: Gherardi F, Holdich DM (eds) Crayfish in Europe as alien species. How to make the best of a bad situation, AA Balkema, Rotterdam, pp 193–219Google Scholar
  61. Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (2006) Atlas of Crayfish in Europe. Patrimoines naturels, 64. Muséum national d’Histoire naturelle, ParisGoogle Scholar
  62. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688PubMedCrossRefGoogle Scholar
  63. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496PubMedCrossRefGoogle Scholar
  64. Tulonen J, Erkamo E, Mannonen A, Jussila J (2010) Juvenile noble crayfish (Astacus astacus) mortality under conditions of water level regulation and predator pressure. Freshwater Crayfish 17:135–140Google Scholar
  65. Tuusti J, Taugbøl T, Skurdal J, Kukk L (1998) Freshwater crayfish in Estonia. Action plan for crayfish management. II: Crayfish status report. Østlandsforskning, rapport 22Google Scholar
  66. van Oosterhout C, Weetman D, Hutchison WF (2006) Estimation and adjustment of microsatellite null alleles in non-equilibrium populations. Mol Ecol Notes 6:255–256CrossRefGoogle Scholar
  67. Wutz S, Geist J (2013) Sex- and size-specific migration patterns and habitat preferences of invasive signal crayfish (Pacifastacus leniusculus Dana). Limnologica 43:59–66CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Riho Gross
    • 1
  • Stefan Palm
    • 2
  • Kuldar Kõiv
    • 1
  • Tore Prestegaard
    • 2
  • Japo Jussila
    • 3
  • Tiit Paaver
    • 1
  • Juergen Geist
    • 4
  • Harri Kokko
    • 3
  • Anna Karjalainen
    • 3
  • Lennart Edsman
    • 2
  1. 1.Department of AquacultureInstitute of Veterinary Medicine and Animal Sciences, Estonian University of Life SciencesTartuEstonia
  2. 2.Department of Aquatic ResourcesInstitute of Freshwater Research, Swedish University of Agricultural SciencesDrottningholmSweden
  3. 3.Department of BiologyUniversity of Eastern FinlandKuopioFinland
  4. 4.Aquatic Systems Biology Unit, Department of Ecology and Ecosystem ManagementTechnische Universität München FreisingGermany

Personalised recommendations