Phylogeography and limited distribution of the endangered freshwater crayfish, Euastacus urospinosus
Charlotte R. Hurry A B , Daniel J. Schmidt A and Jane M. Hughes A
+ Author Affiliations
- Author Affiliations
A Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia.
B Corresponding author. Email: charlotte.hurry@griffithuni.edu.au
Australian Journal of Zoology 63(4) 236-244 https://doi.org/10.1071/ZO15006
Submitted: 17 February 2015 Accepted: 28 August 2015 Published: 23 September 2015
Abstract
Conservation plans can benefit from understanding patterns of genetic structure because many endangered species are spatially fragmented. In particular, headwater species in high elevations are expected to exhibit a high level of population structure, as dispersal through lowland streams may be limited. Euastacus urospinosus is an endangered freshwater crayfish that, until recently, was thought to have a distribution of just 200 km2. In the current study, we identified a total of 26 locations for this species across a 1225 km2 region spanning the Brisbane and Mary River catchments of south-east Queensland, Australia. We then used mitochondrial DNA sequence data to investigate the population structure and the phylogeographic divergence between four uplands. We found significant population differentiation for this species, which conforms to the headwater model of genetic structure. Further, we found that fragmentation between these uplands is most likely historical, as the first divergence between lineages dated back 2.1 million years. Overall, we found no reason to remove the conservation rating of ‘endangered’ for this species. Conservation plans should seek to preserve the genetic integrity of these uplands by considering them to be genetically distinct and isolated populations.
Additional keywords: Cherax leckii, genetic structure, headwater model, phylogenetic, phylogeographic divergence.
References
Aljanabi, S. M., and Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692–4693.| Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsFWrsA%3D%3D&md5=75471f3889d46d8603982d4dddaceb11CAS | 9358185PubMed |
Apte, S., Smith, P. J., and Wallis, G. P. (2007). Mitochondrial phylogeography of New Zealand freshwater crayfishes, Paranephrops spp. Molecular Ecology 16, 1897–1908.
| Mitochondrial phylogeography of New Zealand freshwater crayfishes, Paranephrops spp.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s3js1Gisg%3D%3D&md5=9d496c1b3eeaaf40a0eefb9a460dc00cCAS | 17444900PubMed |
Bensasson, D., Zhang, D. X., Hartl, D. L., and Hewitt, G. M. (2001). Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology & Evolution 16, 314–321.
| Mitochondrial pseudogenes: evolution’s misplaced witnesses.Crossref | GoogleScholarGoogle Scholar |
Bentley, A. I., Schmidt, D. J., and Hughes, J. M. (2010). Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot. Freshwater Biology 55, 1861–1873.
| Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Bernays, S. J., Schmidt, D. J., Hurwood, D. A., and Hughes, J. M. (2015). Phylogeography of two freshwater prawn species from far-northern Queensland. Marine and Freshwater Research 66, 256–266.
| Phylogeography of two freshwater prawn species from far-northern Queensland.Crossref | GoogleScholarGoogle Scholar |
Borsboom, A. (1998). Aspects of the biology and ecology of the Australian freshwater crayfish, Euastacus urospinosus (Decapoda: Parastacidae). Proceedings of the Linnean Society of New South Wales 119, 87–100.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A., and Drummond, A. J. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar | 24722319PubMed |
Bratby, S. (2004). Past and present patterns of dispersal in five species of spiny mountain crayfish of the genus Euastacus (Decapoda: Parastacidae): inferences from mitochondrial data. Honours thesis, Griffith University, Brisbane.
Bryant, D., Crowther, D., and Papas, P. (2012). Improving survey methods and understanding the effects of fire on burrowing and spiny crayfish in the Bunyip and South Gippsland catchments. Black Saturday Victoria (2009) – Natural values fire recovery program. Victorian Government Department of Sustainability and Environment, Melbourne.
Caballero, A., Rodríguez-Ramilo, S., Avila, V., and Fernández, J. (2010). Management of genetic diversity of subdivided populations in conservation programmes. Conservation Genetics 11, 409–419.
| Management of genetic diversity of subdivided populations in conservation programmes.Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=227122fdc40dc723356f66531e13c435CAS | 11050560PubMed |
Cook, B. D., Page, T. J., and Hughes, J. M. (2008). Importance of cryptic species for identifying ‘representative’ units of biodiversity for freshwater conservation. Biological Conservation 141, 2821–2831.
| Importance of cryptic species for identifying ‘representative’ units of biodiversity for freshwater conservation.Crossref | GoogleScholarGoogle Scholar |
Coughran, J., and Furse, J. (2010). An assessment of genus Euastacus (49 species) versus IUCN Red List criteria. Report prepared for the global species conservation assessment of crayfishes for the IUCN Red List of Threatened Species. The Environmental Futures Centre, Griffith School of Environment, Griffith University, Australia.
Doak, N. C. (2005). Phylogeography, dispersal and movement of Fleay’s barred frog, Mixophyes fleayi. Ph.D. thesis, Griffith University, Brisbane.
Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
| Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=7e104a73a8ab14d8d5a8d8a04d4354faCAS | 22367748PubMed |
Excoffier, L., and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| 21565059PubMed |
Fetzner, J. W. J., and Crandall, K. A. (2002). Genetic variation. In ‘Biology Of Freshwater Crayfish’. (Ed. D. M. Holdich.) pp. 291–326. (Blackwell Science: Nottingham, UK.)
Finn, D. S., Blouin, M. S., and Lytle, D. A. (2007). Population genetic structure reveals terrestrial affinities for a headwater stream insect. Freshwater Biology 52, 1881–1897.
| Population genetic structure reveals terrestrial affinities for a headwater stream insect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2qsL7J&md5=037d9d3610af5a2bc08707883513f3d7CAS |
Finn, D. S., Bonada, N., Múrria, C., and Hughes, J. M. (2011). Small but mighty: headwaters are vital to stream network biodiversity at two levels of organization. Journal of the North American Benthological Society 30, 963–980.
| Small but mighty: headwaters are vital to stream network biodiversity at two levels of organization.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=8064cc2c8762aa233192841aec5cffa5CAS | 7881515PubMed |
Fu, Y.-X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 1:STN:280:DyaK2svns1egtQ%3D%3D&md5=80b530fb52e6b80a3e857fe11004844dCAS | 9335623PubMed |
Furse, J, Wild, C, and Villamar, N (2004). In-stream and terrestrial movements of Euastacus sulcatus in the Gold Coast hinterland: developing and testing a method of assessing freshwater crayfish movements. Freshwater Crayfish 14, 213–220.
Grandjean, F., Harris, D. J., Souty-Grosset, C., and Crandall, K. A. (2000). Systematics of the European endangered crayfish species Austropotamobius pallipes (Decapoda, Astacidae). Journal of Crustacean Biology 20, 522–529.
| Systematics of the European endangered crayfish species Austropotamobius pallipes (Decapoda, Astacidae).Crossref | GoogleScholarGoogle Scholar |
Grandjean, F., Gouin, N., Souty-Grosset, C., and Dieguez-Uribeondo, J. (2001). Drastic bottlenecks in the endangered crayfish species Austropotamobius pallipes in Spain and implications for its colonization history. Heredity 86, 431–438.
| Drastic bottlenecks in the endangered crayfish species Austropotamobius pallipes in Spain and implications for its colonization history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsVyjsLs%3D&md5=7e8ada36869389478fe7e5a331c094e0CAS | 11520343PubMed |
Grandjean, F., Frelon-Raimond, M., and Souty-Grosset, C. (2002). Compilation of molecular data for the phylogeny of the genus Austropotamobius: one species or several? Bulletin Francais de la Peche et de la Pisciculture 367, 671–680.
| Compilation of molecular data for the phylogeny of the genus Austropotamobius: one species or several?Crossref | GoogleScholarGoogle Scholar |
Hodges, K., Donnellan, S., and Georges, A. (2014). Phylogeography of the Australian freshwater turtle Chelodina expansa reveals complex relationships among inland and coastal bioregions. Biological Journal of the Linnean Society. Linnean Society of London 111, 789–805.
| Phylogeography of the Australian freshwater turtle Chelodina expansa reveals complex relationships among inland and coastal bioregions.Crossref | GoogleScholarGoogle Scholar |
Hoffmann, A, Griffin, P, Dillon, S, Catullo, R, Rane, R, Byrne, M, Jordan, R, Oakeshott, J, Weeks, A, Joseph, L, Lockhart, P, Borevitz, J, and Sgro, C (2015). A framework for incorporating evolutionary genomics into biodiversity conservation and management. Climate Change Responses 2, 1–24.
Hughes, J. M. (2007). Constraints on recovery: using molecular methods to study connectivity of aquatic biota in rivers and streams. Freshwater Biology 52, 616–631.
| Constraints on recovery: using molecular methods to study connectivity of aquatic biota in rivers and streams.Crossref | GoogleScholarGoogle Scholar |
Hughes, J. M., Bunn, S. E., Kingston, D. M., and Hurwood, D. A. (1995). Genetic differentiation and dispersal among populations of Paratya australiensis (Atyidae) in rainforest streams in southeast Queensland, Australia. Journal of the North American Benthological Society 14, 158–173.
| Genetic differentiation and dispersal among populations of Paratya australiensis (Atyidae) in rainforest streams in southeast Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2Mzos1Sksg%3D%3D&md5=53baa794b74e8315e996551c6d0e922aCAS |
Hughes, J. M., Schmidt, D. J., and Finn, D. S. (2009). Genes in streams: using DNA to understand the movement of freshwater fauna and their riverine habitat. Bioscience 59, 573–583.
| Genes in streams: using DNA to understand the movement of freshwater fauna and their riverine habitat.Crossref | GoogleScholarGoogle Scholar |
Hughes, J. M., Huey, J. A., and Schmidt, D. J. (2013). Is realised connectivity among populations of aquatic fauna predictable from potential connectivity? Freshwater Biology 58, 951–966.
| Is realised connectivity among populations of aquatic fauna predictable from potential connectivity?Crossref | GoogleScholarGoogle Scholar |
Hurry, C. R., Schmidt, D. J., Ponniah, M, Carini, G, Blair, D, and Hughes, J. M. (2014). Shared phylogeographic patterns between the ectocommensal flatworm Temnosewellia albata and its host, the endangered freshwater crayfish Euastacus robertsi. PeerJ 2, e552.
| Shared phylogeographic patterns between the ectocommensal flatworm Temnosewellia albata and its host, the endangered freshwater crayfish Euastacus robertsi.Crossref | GoogleScholarGoogle Scholar | 25279257PubMed |
Hurwood, D. A., Hughes, J., Bunn, S., and Cleary, C. (2003). Population structure in the freshwater shrimp (Paratya australiensis) inferred from allozymes and mitochondrial DNA. Heredity 90, 64–70.
| Population structure in the freshwater shrimp (Paratya australiensis) inferred from allozymes and mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFOntQ%3D%3D&md5=1c48fb602df50540dfc5fa5cb16f640eCAS | 12522427PubMed |
IUCN (2015). The IUCN Red List of Threatened Species. Version 2014.3. <http://www.iucnredlist.org>. Accessed 17 January 2015.
Ketmaier, V., Argano, R., and Caccone, A. (2003). Phylogeography and molecular rates of subterranean aquatic stenasellid isopods with a peri-Tyrrhenian distribution. Molecular Ecology 12, 547–555.
| Phylogeography and molecular rates of subterranean aquatic stenasellid isopods with a peri-Tyrrhenian distribution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FivVyisA%3D%3D&md5=6cc1dc1a2e3ac86d4db1ea3aa0f86c4eCAS | 12535105PubMed |
Larson, E. R., Abbott, C. L., Usio, N., Azuma, N., Wood, K. A., Herborg, L., and Olden, J. D. (2012). The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific northwest range of Pacifastacus leniusculus. Freshwater Biology 57, 1823–1838.
| The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific northwest range of Pacifastacus leniusculus.Crossref | GoogleScholarGoogle Scholar |
Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=2a8dd22e66d8894ea8d3c8b0171bdb3cCAS | 19346325PubMed |
Mathews, L. M., Adams, L., Anderson, E., Basile, M., Gottardi, E., and Buckholt, M. A. (2008). Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex. Molecular Phylogenetics and Evolution 48, 126–135.
| Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntlCktLg%3D&md5=9fc378b56eb2a45aba136144f39f9b59CAS | 18346914PubMed |
McCormack, R. B. 2012. ‘A Guide to Australia’s Spiny Freshwater Crayfish.’ (CSIRO Publishing: Melbourne.)
McCormack, R. B., and Van Der Werf, P. (2013). The distribution, ecology and conservation status of Euastacus urospinosus Riek, 1956 (Crustacea: Decapoda: Parastacidae), a dwarf freshwater crayfish from the Mary and Brisbane River drainages, south-eastern Queensland. Memoirs of the Queensland Museum Nature 56, 639–646.
Miller, A. D., Sweeney, O. F., Whiterod, N. S., Van Rooyen, A. R., Hammer, M., and Weeks, A. R. (2014). Critically low levels of genetic diversity in fragmented populations of the endangered Glenelg spiny freshwater crayfish Euastacus bispinosus. Endangered Species Research 25, 43–55.
| Critically low levels of genetic diversity in fragmented populations of the endangered Glenelg spiny freshwater crayfish Euastacus bispinosus.Crossref | GoogleScholarGoogle Scholar |
Mills, B., McCloud, P., and Huner, J. (1994). Cultivation of freshwater crayfishes in Australia. In ‘Freshwater CrayFish Aquaculture in North America, Europe, and Australia. Families Astacidae, Cambaridae, Parastacidae’. (Ed. J. Huner.) pp. 217–289. (Food Products Press: New York.)
Morgan, G. J. (1988). Freshwater crayfish of the genus Euastacus Clark (Decapoda: Parastacidae) from Queensland. Memoirs of the Museum of Victoria 49, 1–49.
Múrria, C., and Hughes, J. M. (2008). Cyclic habitat displacements during Pleistocene glaciations have induced independent evolution of Tasimia palpata populations (Trichoptera: Tasimiidae) in isolated subtropical rain forest patches. Journal of Biogeography 35, 1727–1737.
| Cyclic habitat displacements during Pleistocene glaciations have induced independent evolution of Tasimia palpata populations (Trichoptera: Tasimiidae) in isolated subtropical rain forest patches.Crossref | GoogleScholarGoogle Scholar |
Norrocky, M. J. (1984). Burrowing crayfish trap. The Ohio Journal of Science 84, 65–66.
Ponniah, M., and Hughes, J. M. (2004). The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA. Evolution 58, 1073–1085.
| The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 15212388PubMed |
Ponniah, M., and Hughes, J. M. (2006). The evolution of Queensland spiny mountain crayfish of the genus Euastacus. II. Investigating simultaneous vicariance with intraspecific genetic data. Marine and Freshwater Research 57, 349–362.
| The evolution of Queensland spiny mountain crayfish of the genus Euastacus. II. Investigating simultaneous vicariance with intraspecific genetic data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFGgsrw%3D&md5=8667341f9e6485c985c094a370240f14CAS |
Quan, A. S., Pease, K. M., Breinholt, J. W., and Wayne, R. K. (2014). Origins of the invasive red swamp crayfish (Procambarus clarkii) in the Santa Monica mountains. Aquatic Invasions 9, 211–219.
| Origins of the invasive red swamp crayfish (Procambarus clarkii) in the Santa Monica mountains.Crossref | GoogleScholarGoogle Scholar |
Sala, O. E., Stuart Chapin, F., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., Kinzig, A., Leemans, R., Lodge, D. M., Mooney, H. A., Oesterheld, M. N., Poff, N. L., Sykes, M. T., Walker, B. H., Walker, M., and Wall, D. H. (2000). Global biodiversity scenarios for the Year 2100. Science 287, 1770–1774.
| Global biodiversity scenarios for the Year 2100.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVWltLk%3D&md5=d29a23bf0b6691b14afc2373634dd31dCAS | 10710299PubMed |
Shull, H. C., Perez-Losada, M., Blair, D., Sewell, K., Sinclair, E. A., Lawler, S., Ponniah, M., and Crandall, K. A. (2005). Phylogeny and biogeography of the freshwater crayfish Euastacus (Decapoda: Parastacidae) based on nuclear and mitochondrial DNA. Molecular Phylogenetics and Evolution 37, 249–263.
| Phylogeny and biogeography of the freshwater crayfish Euastacus (Decapoda: Parastacidae) based on nuclear and mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVart7jE&md5=fddeccdf8b972445b2a7fece5088fa62CAS | 16029952PubMed |
Smith, G., Borsboom, A., Lloyd, R., Lees, N., and Kehl, J. (1998). Habitat changes, growth and abundance of juvenile giant spiny crayfish Euastacus hystricosus (Decapoda: Parastacidae), in the Conondale Ranges, south-east Queensland. Proceedings of the Linnean Society of New South Wales 119, 71–86.
Song, H., Buhay, J. E., Whiting, M. F., and Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105, 13 486–13 491.
| Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChs7vP&md5=daeec132301fa133f19c97e844c2d60fCAS |
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 1:CAS:528:DyaK3cXhslentA%3D%3D&md5=dfad590d42d79769e61b1fb7cb6faf2bCAS | 2513255PubMed |
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=61fd3bd9e6c18850ddc55d16af549242CAS | 24132122PubMed |
Woodward, G., Perkins, D. M., and Brown, L. E. (2010). Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 2093–2106.
| Climate change and freshwater ecosystems: impacts across multiple levels of organization.Crossref | GoogleScholarGoogle Scholar | 20513717PubMed |
