Aquatic Living Resources

Research Article

Population genetic studies on the Australian freshwater crayfish, Cherax destructor (Crustacea: Parastacidae) using allozyme and RAPD markers

Étude de la diversité génétique des populations de l’écrevisse australienne, Cherax destructor (Crustacés : Parastacidés) par les allozymes et les marqueurs RAPD

Thuy T. T. Nguyena1a2, Burridge, Christopher P.a1 and Austin, Christopher M.a1

a1 School of Ecology and Environment, Deakin University, Warrnambool, VIC 3280, Australia

a2 Network of Aquaculture Centres in Asia-Pacific, PO Box 1040, Kasetsart Post Office, Bangkok 10903, Thailand

Abstract

Allozyme and Random Amplified Polymorphic DNA (RAPD) variation was surveyed in the freshwater crayfish Cherax destructor Clark, an ecologically and commercially important species that is widespread throughout the freshwater systems of central Australia. At the intra-population level, allozymes revealed a similar level of variation to that found in other freshwater crayfish; RAPDs showed less diversity than allozymes, which was unexpected. At the inter-population level, both techniques revealed significant population structure, both within and between drainages. RAPD results were consistent with phylogeographic patterns previously identified using mtDNA. Although allozyme data showed little geographic pattern in relation to genetic variation based on multidimensional-scaling (MDS) plots on matrices of genetic distance, results of AMOVA and Mantel tests indicated significant population structuring. Each of the mtDNA lineages proposed in a previous study also showed significant genetic structure at similar levels as revealed by RAPDs but different levels by allozymes. These results reject hypotheses previously put forward on genetic homogenisation within the species due to wide-scale translocation. The implications of the findings for conservation and aquaculture of C. destructor are also discussed.

Résumé

Le polymorphisme des allozymes et des marqueurs RAPD est étudié chez l'écrevisse Cherax destructor Clark, espèce d'importance écologique et commerciale et qui est largement répandue dans tous les bassins hydrographiques de l'Australie centrale. A l'intérieur des populations, les allozymes révèlent un niveau similaire de variation à celui trouvé chez d'autres écrevisses; les marqueurs RAPD montrent moins de diversité que les allozymes, ce qui est inattendu. Entre les populations, les deux techniques révèlent une structure génétique significative, à la fois au sein d'un même bassin hydrographique et entre bassins hydrographiques. Les résultats obtenus avec les marqueurs RAPD révèlent les mêmes relations phylogéographiques identifiées antérieurement par étude de l'ADNmt. Bien que les données allozymiques révèlent peu de structure géographique en relation avec la variation génétique, basée sur l'analyse en composantes principales et le positionnement multidimensionnel (MDS) des matrices des distances génétiques, les résultats des tests AMOVA et de Mantel indiquent une structure significative des populations. Chacune des lignées d'ADNmt proposées dans une précédente étude montre également une structure génétique significative à des niveaux similaires pour les marqueurs RAPD mais différents pour les allozymes. Ces résultats rejettent les hypothèses posées antérieurement sur l'homogénéisation génétique chez cette espèce suite à des translocations réalisées à grande échelle. Les implications de ces résultats pour la protection et l'aquaculture de C. destructor sont aussi discutées.

(Received January 10 2005)

(Accepted February 17 2005)

(Online publication March 15 2005)

Key Words:

  • Population genetics ;
  • Allozymes ;
  • RAPDs ;
  • Cherax destructor

Correspondence:

c1 thuy.nguyen@enaca.org

  • [1] Austin C.M. , 1987, Diversity of Australian freshwater crayfish increase potential for aquaculture. Aust. Fish. 46, 30-31. [1] [OpenURL Query Data]  [Google Scholar]
  • [2] Austin C.M. , 1996, An electrophoretic and morphological taxonomic study of the freshwater crayfish genus Cherax (Decapoda: Parastacidae) in Northern and Eastern Australia. Aust. J. Zool. 44, 259-296. [2] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [3] Austin C.M. , Ryan S. , 2002, Allozyme evidence for a new species of freshwater crayfish of the genus Cherax Erichson (Decapoda: Parastacidae) from the south-west of Western Australia. Invertebr. Syst. 16, 357-367. [3] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [4] Austin C.M. , Nguyen T.T.T. , Meewan M. , Jerry D.R. , 2003, The taxonomy and evolution of the Cherax destructor complex (Decapoda: Parastacidae) rexamined using mitochondrial 16S sequences. Aust. J. Zool. 51, 99-110. [4] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [5] Avery L. , Austin C.M. , 1997, A biochemical taxonomic study of spiny crayfish of the genera Astacopsis and Euastacus (Decapoda: Parastacidae) in south-eastern Australia. Mem. Museum Vict. 56, 543-555. [5] [OpenURL Query Data]  [Google Scholar]
  • [6] Avise J.C., 1994, Molecular Markers, Natural History, and Evolution. Chapman and Hall, New York.
  • [7] Avise J.C., 2000, Phylogeography - The History and Formation of Species. Harvard University Press, USA. [7] [Google Scholar]
  • [8] Avise J.C. , Arnold J. , Martin Ball R. , Bermingham E. , Lamb T. , Neigel J.E. , Reeb C.A. , Saunders N.C. , 1987, Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18, 489-522. [8] [OpenURL Query Data]  [Google Scholar]
  • [9] Bohonak A.J. , 2002, IBD (Isolation by Distance): A program for analyses of isolation by distance. J. Hered. 93, 153-154. [9] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [10] Busack C.A. , 1988, Electrophoretic variation in the red swamp (Procambarus clarkii) and white river crayfish (P. acutus) (Decapoda: Cambaridae). Aquaculture 69, 211-226. [10] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [11] Campbell N.J.H. , Geddes M.C. , Adams M. , 1994, Genetic variation in yabbies, Cherax destructor and C. albidus (Crustacea: Decapoda: Parastacidae), indicates the presence of a single, highly sub-structured species. Aust. J. Zool. 42, 745-760. [11] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [12] Carvalho G.R., Pitcher T.J., 1995, Molecular Genetics in Fisheries. Chapman & Hall.
  • [13] Crandall K.A. , 1997, Genetic variation within and among crayfish species. Freshwater Crayfish 11, 135-145. [13] [OpenURL Query Data]  [Google Scholar]
  • [14] Cross T., Dillance E., Galvin P., 2000, Which molecular markers should be chosen for different specfic applications in fisheries and aquaculture? National University of Ireland.
  • [15] D'Amato M.E. , Corach D. , 1996, Genetic diversity of the freshwater shrimp Macrobrachium borelli (Caridea: Papaemonidae) evaluated by RAPD analysis. J. Crust. Biol. 16, 650-655. [15] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [16] D'Amato M.E. , Corach D. , 1997, Population genetic structure in the freshwater anomuran Aegla jujuyana by RAPD analysis. J. Crust. Biol. 17, 269-274. [16] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [17] Edsman L. , Farris J.S. , 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. 367, 691-706. [17] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [18] Fetzner J.W.J. , 1996, Biochemical systematic and evolution of the crayfish genus Orconectes (Decapoda: Cambaridae). J. Crust. Biol. 116, 111-141. [18] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [19] Fetzner J.W.J. , Crandall K.A. , 1999, Genetic variability within and among populations of the golden crayfish (Orconectes luteus): A comparison using amplified fragment length polymorphisms (AFLPs) and mitochondrial 16S gene sequences. Freshwater Crayfish 12, 386-396. [19] [OpenURL Query Data]  [Google Scholar]
  • [20] Fetzner J.W.J., Crandall K.A., 2001, Genetic Variation. In: Holdich, D.M. (Ed.), Biology of Freshwater Crayfish. Blackwell Science, Oxford, pp. 291-326. [20] [Google Scholar]
  • [21] Fetzner J.W.J. , Sheehan R.J. , Sheeb L.W. , 1997, Genetic implications of broodstock selection for crayfish aquaculture in the Midwestern United States. Aquaculture 154, 39-55. [21] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [22] Fevolden S.E. , Hessen D.O. , 1989, Morphological and genetic differences among recently founded populations of noble crayfish (Astacus astacus). Hereditas 110, 149-158. [22] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [23] Fratini S. , Zaccara S. , Barbaresi S. , Grandjean F. , Souty-Grosset C. , Crosa G. , Gherardi F. , 2005, Phylogeography of the threatened crayfish (genus Austropotamobius) in Italy: Implications for its taxonomy and conservation. Heredity 94, 108-118. [23] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [24] Fuller B. , Lester L.J. , 1980, Correlations of alloymic variation with habitat parameters using the grass shrimp, Palaemonetes pugio. Evolution 34, 1099-1104. [24] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [25] Goudet J., 2001, FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995).
  • [26] Gouin N. , Grandjean F. , Bouchon D. , Reynolds J.D. , Souty-Grosset C. , 2001, Population genetic structure of the endangered freshwater crayfish Austropotamobius pallipes, assessed using RAPD markers. Heredity 87, 80-87. [26] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [27] Gouin N. , Grandjean F. , Pain S. , Souty-Grosset C. , Reynolds J. , 2003, Origin and colonization history of the white-clawed crayfish, Austrapotamobius pallipes, in Ireland. Heredity 91, 70-77. [27] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [28] Grandjean F., Gouin, N., Souty-Grosset, C., Dieguez-Uribeondo, J. 2001, Drastic bottlenecks in the endangered crayfish species Austropotamobius pallipes in Spain with reference to its colonisation history. Heredity 86, 431-438.
  • [29] Hebert P.D.N., Beaton M.J., 1993, Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories.
  • [30] Hedgecock D. , Stelmach D.J. , Nelson K. , Lindenfelser M.E. , Malecha S.R. , 1979, Genetic divergence and biogeography of natural populations of Macrobrachium rosenbergii. Proc. World Maricult. Soc. 10, 873-879. [30] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [31] Hellberg M.E. , 1994, Relationships between inferred level of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48, 1829-1854. [31] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [32] Horwitz P. , Knott B. , 1995, The distribution and spread of the yabby Cherax complex in Australia: Speculations, hypotheses and the need for research. Freshwater Crayfish 10, 81-91. [32] [OpenURL Query Data]  [Google Scholar]
  • [33] Hughes J.M. , Hillyer M.J. , 2003, Patterns of connectivity among populations of Cherax destructor (Decapoda: Parastacidae) in western Queensland, Australia. Mar. Freshwater Res. 54, 587-596. [33] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [34] Jerry D.R. , Purvis I.W. , Piper L.R. , 2002, Genetic differences in growth among wild populations of the yabby, Cherax destructor Clark. Aquac. Res. 33, 917-923. [34] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [35] Johnson M.S. , 2000, Measuring and intepreting genetic structure to minimise the genetic risk of translocation. Aquac. Res. 31, 133-143. [35] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [36] Karl S.A. , Avise J.C. , 1992, Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256, 100-102. [36] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [37] Karl S.A. , Bowen B. , Avise J.C. , 1992, Global population structure and male-mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear loci. Genetics 131, 163-173. [37] [OpenURL Query Data]  [Google Scholar]
  • [38] Lawrence C.S. , Morrissy N.M. , 2000, Genetic improvement of marron Cherax tenuimanus Smith and yabbies Cherax spp. in Western Australia. Aquac. Res. 31, 69-82. [38] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [39] Liu Z.J, Li P., Argue B.J., Dunham R.A., 1999, Random amplified polymorphic DNA markers: Usefulness for gene mapping and analysis of genetic variation of catfish. Aquaculture, 174, 59-68.
  • [40] Lörtscher M. , Clauna M. , Scholl A. , 1998, Genetic population structure of Austropotamobius pallipes (Lereboullet 1858) (Decapoda, Astacidae) in Switzerland, based on allozyme data. Aquat. Sci. 60, 118-129. [40] [OpenURL Query Data]  [Google Scholar]
  • [41] Lörtscher M. , Stucki T.P. , Clalüna M. , Scholl A. , 1997, Phylogeographic structure of Austropotamobius pallipes populations in Switzerland. Bull. Fr. Pêche Piscic. 347, 649-661. [41] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [42] Macaranas J.M. , Mather P.B. , Hoeben P. , Capra M.F. , 1995, Assessment of genetic variation in wild populations of the redclaw crayfish (Cherax quadricarinatus von Martens 1868) by means of allozyme and RAPD-PCR markers. Aust. J. Mar. Freshwater Res. 46, 1217-1228. [42] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [43] Merrick J.R., Lambert C.N., 1991, The Yabby, Marron and Redclaw Production and Marketing. Macathur Press, Parramatta, N. S. W., Australia. [43] [Google Scholar]
  • [44] Moritz C. , 1994, Applications of mitochondrial DNA analysis in conservation: a critical review. Mol. Ecol. 3, 401-411. [44] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [45] Moritz C. , 2002, Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51, 238-254. [45] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [46] Moritz C., Hillis D.M., 1996, Molecular systematics: Context and controversies. In: Hillis D.M., Moritz C., Mable B.K. (Eds.), Molecular Systematics. Sinauer Associates, Inc., Sunderland, MA, pp. 1-13. [46] [Google Scholar]
  • [47] Morrissy N.M. , Evans L. , Huner J.V. , 1990, Australian freshwater crayfish: Aquaculture species. World Aquac. 21, 113-120. [47] [OpenURL Query Data]  [Google Scholar]
  • [48] Nevo E.T., Belles A., Shlomo B., 1984, The evolutionary significance of genetic diversity: Ecological, demographic and life history correlates. In: Mani G.S. (Ed.), Evolutionary Dynamics of Genetic Diversity. Springer, Berlin, pp. 14-213. [48] [Google Scholar]
  • [49] Nguyen T.T.T., 2004, Molecular genetic studies of the yabby, Cherax destructor Clark. PhD Thesis, School of Ecology and Environment, Deakin University, Australia.
  • [50] Nguyen T.T.T. , Austin C.M. , 2004, Inheritance of molecular markers and sex in the Australian freshwater crayfish, Cherax destructor Clark. Aquac. Res. 35, 1328-1338. [50] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [51] Nguyen T.T.T. , Austin C.M. , Meewan M. , Jerry D.R. , 2004, Phylogeography of the freshwater crayfish Cherax destructor Clark (Parastacidae) in inland Australia: Historical fragmentation and recent range expansion. Biol. J. Linn. Soc. 83, 539-550. [51] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [52] Palumbi S. , Baker C.S. , 1994, Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Mol. Biol. Evol. 11, 426-435. [52] [OpenURL Query Data]  [Google Scholar]
  • [53] Peakall R., Smouse P.E., 2003, GenAlEx V5.1: Genetic Analysis in Excel. Population gentic software for teaching and research. Australian National University, Canberra.
  • [54] Peakall R. , Smouse P.E. , Huff D.R. , 1995, Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloe dactyloides. Mol. Ecol. 4, 135-147. [54] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [55] Perry W.L., Feder J.L., Lodge D.M., 2001,. Implications of hybridisation between introduced and resident Orconectes crayfishes. Conserv. Biol. 15, 1656-1666.
  • [56] Perry W.L. , Feder J.L. , Dwyer G. , Lodge D.M. , 2001, Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution 55, 1153-1166. [56] [OpenURL Query Data]  [Google Scholar]
  • [57] Perry W.L. , Lodge D.M. , Feder J.L. , 2002, Importance of hybridisation between indigenous and non-indigenous freshwater species: an overlooked threat to North American biodiversity. Syst. Biol. 51, 255-275. [57] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [58] Raymond M. , Rousset F. , 1995, GENEPOP: Population genetic software for exact test ecumenicism. J. Hered. 86, 248-249. [58] [OpenURL Query Data]  [Google Scholar]
  • [59] Reeb C.A. , Avise J.C. , 1990, A genetic discontinuity in continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124, 397-406. [59] [OpenURL Query Data]  [Google Scholar]
  • [60] Richardson B.J., Baverstock P.R., Adams M., 1986, Allozyme Electrophoresis: A Handbook for Animal Systematics and Population Studies. Academic Press, Australia. [60] [Google Scholar]
  • [61] Rogers J.S., 1972, Measures of genetic similartiy and genetic distance, Studies in Genetics VII. University of Texas Publication No. 7213, Austin.
  • [62] Ryman N. , Jorde P.E. , 2001, Statistical power when testing for genetic differentiation. Mol. Ecol. 10, 2361-2373. [62] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [63] Santucci F. , Iaconelli M. , Andreani P. , Cianchi R. , Nascetii G. , Bullini L. , 1997, Allozyme diversity of European freshwater crayfish of the genus Austropotamobius. Bull. Fr. Pêche Piscic. 347, 663-676. [63] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [64] 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. [64] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [65] Skroch P. , Nienhuis J. , 1995, Impact of scoring error and reproducibility of RAPD data on RAPD based estimates of genetic distance. Theor. Appl. Genet. 91, 1086-1092. [65] [OpenURL Query Data]  [Google Scholar]
  • [66] Sokol A., 1988, Morphological variation in relation to the taxonomy of the destructor group of the genus Cherax. Invertebr. Taxon. 2: 55-79.
  • [67] Souty-Grosset C. , Grandjean F. , Gouin N. , 1999, Molecular genetic contributions to conservation biology of the European native crayfish Austropotamobius pallipes. Freshwater Crayfish 12, 371-386. [67] [OpenURL Query Data]  [Google Scholar]
  • [68] Ward R.D. , Woodwark M. , Skibinski D.O.F. , 1994, A comparison of genetic diversity in marine, freshwater and anadromous fishes. J. Fish Biol. 44, 213-232. [68] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [69] Weir B.S. , Cockerham C.C. , 1984, Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370. [69] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [70] Wilson A.C. , Cann R.L. , Carr S.M. , George M. , Gyllensten U.B. , Helm-Bychowski K. , Higuchi R.G. , Palumbi S.R. , Prager E.M. , Sage R.D. , Stoneking M. , 1985, Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26, 375-400. [70] [OpenURL Query Data]  [CrossRef]  [Google Scholar]
  • [71] Wright S., 1978, Evolution and the genetics of populations, Vol. 4, Variability within and among natural populations. Chicago: University of Chicago Press.
  • [72] Yeh F.C., Yang R.-C., Boyle T., 1999, PopGene Version 1.3.1: Microsoft Windows-based Freeware for Population Genetic Analysis.