Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 113:101–108

    Article  Google Scholar 

  • 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 380–381:965–976

    Article  Google Scholar 

  • Alaranta A, Jussila J, Kokko H (2011) Inheritance of ITS1 region microsatellite-like repeats in the noble crayfish, Astacus astacus (Decapoda, Astacidea). Crustaceana 84:1325–1336

    Article  Google Scholar 

  • Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Alm G (1929) Der Krebs und die Krebspest in Schweden. Zeitschrift für Fisherei 27:123–138 (in German)

    Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–451

    Article  Google Scholar 

  • 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 380–381:1291–1302

    Article  Google Scholar 

  • 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 133–149

    Google Scholar 

  • Edsman L (2004) The Swedish story about import of live crayfish. Bull Fr Pêche Piscic 372–373:281–288

    Article  Google Scholar 

  • Edsman L, Schröder S (2009) Action plan for noble crayfish 2008–2013 (Astacus astacus). Fiskeriverket och Naturvårdsverket, Rapport 5955 (In Swedish with English summary)

  • 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 36:691–706

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Farkac J, Král D, Škorpík M (eds) (2005) List of threatened species in the Czech Republic. Invertebrates, Agentura ochrany prírody a krajiny CR, Praha

    Google Scholar 

  • 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 25:927–935

    Article  Google Scholar 

  • Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005) Candidate genes for behavioural ecology. Trends Ecol Evol 20:96–104

    Article  PubMed  Google Scholar 

  • 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 25–48

    Google Scholar 

  • 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

  • Geist J (2011) Integrative freshwater ecology and biodiversity conservation. Ecol Ind 11:1507–1516

    Article  Google Scholar 

  • 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

  • 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 87:80–87

    Article  PubMed  CAS  Google Scholar 

  • 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 51:1369–1387

    Article  CAS  Google Scholar 

  • Grandjean F, Souty-Grosset C (2000) Mitochondrial DNA variation and population genetic structure of the white-clawed crayfish, Austropotamobius pallipes pallipes. Cons Genet 1:309–319

    Article  CAS  Google Scholar 

  • 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 43:210–220

    Article  PubMed  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Gydemo R, Gydemo R (1990). Utsättningar av flodkräfta i Västerbottens län. Rapport Swedish University of Agricultural Sciences, Department of Aquaculture, 4 (In Swedish)

  • Hansen MM, Meier K, Mensberg K-LD (2010) Identifying footprints of selection in stocked brown trout populations: a spatio-temporal approach. Mol Ecol 19:1787–1800

    Article  PubMed  Google Scholar 

  • 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 17:284–291

    Article  PubMed  CAS  Google Scholar 

  • 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 99:592–600

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • 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 394–395:11

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • 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 2:258–271

    Article  PubMed  Google Scholar 

  • Jussila J, Mannonen A (2004) Crayfisheries in Finland, a short overview. Bull Fr Pêche Piscic 372–373:263–274

    Article  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kõiv K, Gross R, Paaver T, Kuehn R (2008) Isolation and characterization of first microsatellite markers for the noble crayfish, Astacus astacus. Cons Genet 9:1703–1706

    Article  Google Scholar 

  • 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 40:124–126

    Article  PubMed  Google Scholar 

  • 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 88:391–401

    Article  PubMed  CAS  Google Scholar 

  • Laikre L, Ryman N (1996) Effects on intraspecific biodiversity from harvesting and enhancing natural populations. Ambio 25:504–509

    Google Scholar 

  • Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19:4293

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170

    Article  PubMed  CAS  Google Scholar 

  • 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 8:1387–1404

    Article  PubMed  Google Scholar 

  • 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 10:89–102

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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 209–221

    Google Scholar 

  • Paaver T, Hurt M (2009) Status and management of noble crayfish Astacus astacus in Estonia. Knowl Manage Aquat Ecosyst 344–345:42–45

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995a) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Reynolds J, Souty-Grosset C (2012) Management of freshwater biodiversity: crayfish as bioindicators. Cambridge University Press, New York

    Google Scholar 

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

    Article  Google Scholar 

  • 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 62:1887–1904

    Article  Google Scholar 

  • 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 147:205–214

    Article  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • 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 347:663–676

    Article  Google Scholar 

  • 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 401:35p1–35p14

    Google Scholar 

  • 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 356:123–138

    Article  Google Scholar 

  • 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 372–373:387–399

    Article  Google Scholar 

  • 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 193–219

    Google Scholar 

  • 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, Paris

  • Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688

    Article  PubMed  CAS  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • 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 17:135–140

    Google Scholar 

  • Tuusti J, Taugbøl T, Skurdal J, Kukk L (1998) Freshwater crayfish in Estonia. Action plan for crayfish management. II: Crayfish status report. Østlandsforskning, rapport 22

  • van Oosterhout C, Weetman D, Hutchison WF (2006) Estimation and adjustment of microsatellite null alleles in non-equilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  • Wutz S, Geist J (2013) Sex- and size-specific migration patterns and habitat preferences of invasive signal crayfish (Pacifastacus leniusculus Dana). Limnologica 43:59–66

    Article  Google Scholar 

Download references

Acknowledgments

We express gratitude to Mr. Margo Hurt for collecting samples from Estonian crayfish populations, to Dr. Pavel Kozák for providing Czech crayfish samples and to Mr. Hans Lindell for providing background information on Finnish crayfish stocks. The work by R. Gross, K. Kõiv and T. Paaver was financed by the Estonian Science Foundation (Grant No. 7348) and the Estonian Ministry of Education and Research (targeted finance grant SF1080022s07 and institutional research funding project IUT8-2). S. Palm acknowledges funding from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS; Grant No. 215-2010-1235). L. Edsman and T. Prestegaard acknowledge financial support from the Swedish Board of Fisheries. J. Jussila, A. Karjalainen and H. Kokko acknowledge financing from the Ministry of Agriculture and Forestry and the strategic funding of the University of Eastern Finland.

Author information

Authors and Affiliations

  1. Department of Aquaculture, Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Kreutzwaldi 48, 51014, Tartu, Estonia

    Riho Gross, Kuldar Kõiv & Tiit Paaver

  2. Department of Aquatic Resources, Institute of Freshwater Research, Swedish University of Agricultural Sciences, Stångholmsvägen 2, 17893, Drottningholm, Sweden

    Stefan Palm, Tore Prestegaard & Lennart Edsman

  3. Department of Biology, University of Eastern Finland, P.O. Box 1627, 70211, Kuopio, Finland

    Japo Jussila, Harri Kokko & Anna Karjalainen

  4. Aquatic Systems Biology Unit, Department of Ecology and Ecosystem Management, Technische Universität München, Mühlenweg 22, 85354, Freising, Germany

    Juergen Geist

Authors
  1. Riho Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Palm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kuldar Kõiv
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tore Prestegaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Japo Jussila
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tiit Paaver
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Juergen Geist
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Harri Kokko
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anna Karjalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lennart Edsman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Riho Gross.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gross, R., Palm, S., Kõiv, K. et al. Microsatellite markers reveal clear geographic structuring among threatened noble crayfish (Astacus astacus) populations in Northern and Central Europe. Conserv Genet 14, 809–821 (2013). https://doi.org/10.1007/s10592-013-0476-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0476-9

Keywords

Search

Navigation