Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences

Distribution and population genetics of the threatened freshwater crayfish genus Tenuibranchiurus (Decapoda : Parastacidae)

Kathryn L. Dawkins A D , James M. Furse B , Clyde H. Wild B and Jane M. Hughes C

A Australian Rivers Institute, Griffith University, Gold Coast, Qld 4222, Australia.

B Environmental Futures Centre, Griffith University, Gold Coast, Qld 4222, Australia.

C Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia.

D Corresponding author. Email:

Marine and Freshwater Research 61(9) 1048-1055
Submitted: 19 November 2009  Accepted: 30 March 2010   Published: 23 September 2010


Very high rates of extinction are recorded in freshwater ecosystems, with coastally distributed species threatened by urban development, pollution and climate change. One example, the world’s second smallest freshwater crayfish (genus Tenuibranchiurus), inhabits coastal swamps in central-eastern Australia. Although only one species is described (Tenuibranchiurus glypticus), it was expected that populations isolated through habitat fragmentation would be highly divergent. The aims of this study were to determine if populations of Tenuibranchiurus are genetically distinct, and if ancient divergence, as indicated in other species in the region, was evident. Tenuibranchiurus were collected at seven sites, extending the known geographical distribution ~260 km south to Wooli, New South Wales. Analysis of two mitochondrial DNA gene regions indicated two highly divergent clades, with numerous additional subclades. Both clades and subclades were strongly congruent with geographical location, and were estimated to have diverged from each other during the Miocene or Pliocene era. Little sharing of haplotypes between subpopulations was evident, indicating negligible gene flow, and genetic differentiation between subclades possibly indicates distinct species. The coastal distribution of Tenuibranchiurus, severe habitat fragmentation and clear differences between subclades suggest that they should be recognised as evolutionarily significant units, and be treated as such if conservation and management initiatives are warranted.


Austin C. M.Ryan S. G.2002Allozyme evidence for a new species of freshwater crayfish of the genus Cherax Erichson (Decapoda :Parastacidae) from the south-west of Western Australia.Invertebrate Systematics16357367doi:10.1071/IT01010

Baker A. M.Williams S. A.Hughes J. M.2003Patterns of spatial genetic structuring in a hydropsychid caddisfly (Cheumatopsyche sp. AV1) from southeastern Australia.Molecular Ecology1233133324doi:10.1046/J.1365-294X.2003.02011.X

Baker A. M.Hughes J. M.Dean J. C.Bunn S. E.2004Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages.Marine and Freshwater Research55629640doi:10.1071/MF04050

Bentley A. (2007). Phylogeographic structure of freshwater crayfish of the genus Cherax (Decapoda: Parastacidae) on the mainland and islands of southeast Queensland. BSc (Hons) Thesis, Griffith University, Nathan.

Bentley A. I.Schmidt D. J.Hughes J. M.2010Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot.Freshwater Biology5518611873doi:10.1111/J.1365-2427.2010.02420.X

Carini G.Hughes J. M.2004Population structure of Macrobrachium australiense (Decapoda: Palaemonidae) in Western Queensland, Australia: the role of contemporary and historical processes.Heredity93350363doi:10.1038/SJ.HDY.6800510

Chenoweth S. F.Hughes J. M.2003Speciation and phylogeography in Caridina indistincta, a complex of freshwater shrimps from Australian heathland streams.Marine and Freshwater Research54807812doi:10.1071/MF02168

Clement M.Posada D.Crandall K. A.2000TCS: a computer program to estimate gene genealogies.Molecular Ecology916571659doi:10.1046/J.1365-294X.2000.01020.X

Cook B. D.Baker A. M.Page T. J.Grant C.Fawcett J. al.2006Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role of life history transition in phylogeographic diversification.Molecular Ecology1510831093doi:10.1111/J.1365-294X.2006.02852.X

Cook B. D.Page T. J.Hughes J. M.2008aImportance of cryptic species for identifying ‘representative’ units of biodiversity for freshwater conservation.Biological Conservation14128212831doi:10.1016/J.BIOCON.2008.08.018

Cook B. D.Pringle C. M.Hughes J. M.2008bMolecular evidence for sequential colonization and taxon cycling in freshwater decapod shrimps on a Caribbean island.Molecular Ecology1710661075doi:10.1111/J.1365-294X.2007.03637.X

Crandall K. A.2002Crayfish as model organisms.Freshwater Crayfish13310

Crandall K. A.Fetzner J. W.Lawler S. H.Kinnersley M.Austin C. M.1999Phylogenetic relationships among the Australian and New Zealand genera of freshwater crayfishes (Decapoda : Parastacidae).Australian Journal of Zoology47199214

de Bruyn M.Wilson J. A.Mather P. B.2004Huxley’s line demarcates extensive genetic divergence between eastern and western forms of the giant freshwater prawn, Macrobrachium rosenbergii.Molecular Phylogenetics and Evolution30251257doi:10.1016/S1055-7903(03)00176-3

Dieguez-Uribeondo J.Royo F.Souty-Grosset C.Ropiquet A.Grandjean F.2008Low genetic variability of the white-clawed crayfish in the Iberian Peninsula: its origin and management implications.Aquatic Conservation: Marine & Freshwater Ecosystems181931doi:10.1002/AQC.811

Doyle J. J.Doyle J. L.1987A rapid DNA isolation procedure for small quantities of leaf tissue.Phytochemical Bulletin191115

Excoffier L.Laval G.Schneider S.2005Arlequin ver. 3.0: An integrated software package for population genetics data analysis.Evolutionary Bioinformatics Online14750

Fratini S.Zaccara S.Barbaresi S.Grandjean F.Souty-Grosset al.2005Phylogeography of the threatened crayfish (genus Austropotamobius) in Italy: implications for its taxonomy and conservation.Heredity94108118

Fu Y.-X.Li W.-L.1993Statistical tests of neutrality of mutations.Genetics133693709

GeneCodes (2000). ‘Sequencher (Version 4.1.2).’ (Gene Codes Corporation: Ann Arbor, MI.)

Gouin N.Grandjean F.Souty-Grosset C.2006Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications.Freshwater Biology5113691387

Harding D.Williamson I.2003A note on the habitat requirements of the swamp crayfish on Bribie Island, southeastern Queensland.Memoirs of the Queensland Museum49452

Harding D.Williamson I.2004The influence of light phase and predators on the behaviour of swamp crayfish.Memoirs of the Queensland Museum49704

Hartl D. L., and Clark A. G. (2007). ‘Principles of Population Genetics.’ 4th edn. (Sinauer Associates Inc. Publishers: Sunderland, MA.)

Horwitz P. (1995). A preliminary key to the species of Decapoda (Crustacea: Malacostraca) found in Australian inland waters. Co-operative Research Centre for Freshwater Ecology, Albury, Australia.

Hughes J. M.Hillyer M. J.2003Patterns of connectivity among populations of Cherax destructor (Decapoda : Parastacidae) in western Queensland, Australia.Marine and Freshwater Research54587596

Hughes J. M.Ponniah M.Hurwood D. A.Chenoweth S. F.Arthington A.1999Strong genetic structuring in a habitat specialist, the Oxleyan Pygmy Perch Nannoperca oxleyana.Heredity83514doi:10.1038/SJ.HDY.6885390

Jenkins M.2003Prospects for biodiversity.Science30211751177doi:10.1126/SCIENCE.1088666

Joyce K. (2006). ‘Wetland Management Profile: Coastal Melaleuca Swamp Wetlands.’ (Ecosystem Conservation Branch, EPA: Brisbane, Queensland.)

Katoh K.Kuma K.-I.Toh H.Miyata T.2005MAFFT version 5: improvement in accuracy of multiple sequence alignment.Nucleic Acids Research33511518doi:10.1093/NAR/GKI198

Knight J. T.Nock C. J.Elphinstone M. S.Baverstock P. R.2009Conservation implications of distinct genetic structuring in the endangered freshwater fish Nannoperca oxleyana (Percichthyidae).Marine and Freshwater Research603444doi:10.1071/MF08022

Lindqvist O. V., and Huner J. V. (1999). Life history characteristics of crayfish: What makes some of them good colonizers? In ‘Biotic Interactions and Global Change’. (Eds P. Kareiva, J. Kingsolver and R. Huey.) pp. 23–30. (Sinauer Associates Inc.: Sunderland, MA.)

Loh J. (2002). ‘Living. The Planetary Report, 2002.’ (World Wide Fund for Nature International: Gland, Switzerland.)

Margules C. R.Pressey R. L.2000Systematic conservation planning.Nature405243253doi:10.1038/35012251

Mills C. E.Hadwen W. L.Hughes J. M.2008Looking through glassfish: marine genetic structure in an estuarine species.Marine and Freshwater Research59627637doi:10.1071/MF07215

Moritz C.1994Defining ‘evolutionarily significant units’ for conservation.Trends in Ecology & Evolution9373375doi:10.1016/0169-5347(94)90057-4

Morrison C. L.Rios R.Duffy J. E.2004Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus).Molecular Phylogenetics and Evolution30563581doi:10.1016/S1055-7903(03)00252-5

Nguyen T. T. T.Meewan M.Ryan S.Austin C. M.2002Genetic diversity and translocation in the marron, Cherax tenuimanus (Smith): implications for management and conservation.Fisheries Management and Ecology9163173doi:10.1046/J.1365-2400.2002.00289.X

Page T. J.Hughes J. M.2007Phylogeographic structure in an Australian freshwater shrimp largely pre-dates the geological origins of its landscape.Heredity98222231doi:10.1038/SJ.HDY.6800932

Page T. J.Sharma S.Hughes J. M.2004Deep phylogenetic structure has conservation implications for ornate rainbow fish (Melanotaeniidae: Rhadinocentrus ornatus) in Queensland, eastern Australia.Marine and Freshwater Research55165172doi:10.1071/MF03139

Palumbi S. R., Martin A., Romano S., McMillan W. O., Stice L., et al. (1991). ‘The Simple Fool’s Guide to PCR.’ (University of Hawaii Press: Honolulu.)

Ponniah M.Hughes J. M.2004The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA.Evolution5810731085

Posada D.2008jModelTest: Phylogenetic Model Averaging.Molecular Biology and Evolution2512531256

Ricciardi A.Rasmussen J. B.1999Extinction rates of North American freshwater fauna.Conservation Biology1312201222doi:10.1046/J.1523-1739.1999.98380.X

Riek E. F.1951The freshwater crayfish (family Parastacidae) of Queensland, with an appendix describing other Australian species.Records of the Australian Museum22368388

Riek E. F.1969The Australian freshwater crayfish (Crustacea : Decapoda : Parastacidae), with descriptions of new species.Australian Journal of Zoology17855918

Rode A. L.Babcock L. E.2003Phylogeny of fossil and extant freshwater crayfish and some closely related nephropid lobsters.Journal of Crustacean Biology23418435doi:10.1651/0278-0372(2003)023[0418:POFAEF]2.0.CO;2

Santos S. R.2006Patterns of genetic connectivity among anchialine habitats: a case study of the endemic Hawaiian shrimp Halocaridina rubra on the island of Hawaii.Molecular Ecology1526992718

Schubart C. D.Diesel R.Hedges S. B.1998Rapid evolution to terrestrial life in Jamaican crabs.Nature393363365

Schultz M. B.Smith S. A.Richardson A. M. M.Horwitz P.Crandall K. al.2007Cryptic diversity in Engaeus Erichson, Geocharax Clark and Gramastacus Riek (Decapoda : Parastacidae) revealed by mitochondrial 16S rDNA sequences.Invertebrate Systematics21569587doi:10.1071/IS07019

Schultz M. B.Smith S. A.Horwitz P.Richardson A. M. M.Crandall K. al.2009Evolution underground: A molecular phylogenetic investigation of Australian burrowing freshwater crayfish (Decapoda: Parastacidae) with particular focus on Engaeus Erichson.Molecular Phylogenetics and Evolution50580598doi:10.1016/J.YMPEV.2008.11.025

Sharma S.Hughes J. M.2009Genetic structure and phylogeography of freshwater shrimps (Macrobrachium australiense and Macrobrachium tolmerum): the role of contemporary and historical events.Marine and Freshwater Research60541553doi:10.1071/MF07235

Slatkin M.1993Isolation by distance in equilibrium and non-equilibrium populations.Evolution47264279doi:10.2307/2410134

Stamatakis A.2006RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Bioinformatics2226882690doi:10.1093/BIOINFORMATICS/BTL446

Stillman J. H.Reeb C. A.2001Molecular phylogeny of eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications.Molecular Phylogenetics and Evolution19236245doi:10.1006/MPEV.2001.0924

Sturmbauer C.Leninton J. S.Christy J.1996Molecular phylogeny analysis of fiddler crabs: Test of the hypothesis of increasing behavioral complexity in evolution.Proceedings of the National Academy of Sciences of the United States of America9310 85510 857doi:10.1073/PNAS.93.20.10855

Swofford D. L. (2003). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods) (Version 4).’ (Sinauer Associates: Sunderland, MA.)

Tajima F.1989Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.Genetics123585595

Tamura K.Dudley J.Nei M.Kumar S.2007MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.Molecular Biology and Evolution2415961599

Taylor C. A.Schuster G. A.Cooper J. E.DiStefano R. J.Eversole A. al.2007A reassessment of the conservation status of crayfishes of the United States and Canada after 10+ years of increased awareness.Fisheries32372389doi:10.1577/1548-8446(2007)32[372:AROTCS]2.0.CO;2

Wares J. P.Cunningham C. W.2001Phylogeography and historical ecology of the North Atlantic intertidal.Evolution5524552469

Supplementary MaterialSupplementary Material 9.9 KB Export Citation