Species diversity and genetic differentiation of stygofauna (Syncarida : Bathynellacea) across an alluvial aquifer in north-eastern Australia
B. D. Cook A B E , K. M. Abrams C , J. Marshall A , C. N. Perna A , S. Choy A , M. T. Guzik C and S. J. B. Cooper C D
+ Author Affiliations
- Author Affiliations
A Water Planning Ecology, Science Delivery, Queensland Department of Science, Information Technology, Innovation and the Arts, EcoSciences Precinct, 41 Boggo Road, Dutton Park, Qld 4102, Australia.
B Present address: frc environmental Pty Ltd, PO Box 2363, Wellington Point, Qld 4061, Australia.
C Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
D Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
E Corresponding author. Email: bencook@frcenv.com.au
Australian Journal of Zoology 60(3) 152-158 https://doi.org/10.1071/ZO12061
Submitted: 10 June 2012 Accepted: 13 August 2012 Published: 4 October 2012
Abstract
Recent research suggests that alluvial aquifers in southern and eastern Australia may contain a diverse subterranean aquatic fauna (i.e. stygofauna). However, to date only a limited number of alluvial aquifers have been studied and little molecular data are available to assess species-level diversity and spatial patterns of genetic variation within stygofaunal species. In this paper, we present the initial results of a stygofaunal survey of the Burdekin River alluvial aquifer in Queensland, extending the northern range of alluvial aquifers along the east coast of Australia that have been investigated. The survey resulted in the collection of bathynellid stygofauna (Syncarida: Bathynellacea) and genetic analyses were conducted to determine species level diversity using the mitochondrial cytochrome oxidase subunit I (COI) gene. We further investigated the phylogenetic relationships of the species with bathynellids from western and southern Australia to assess the generic status of species. Four highly divergent COI lineages within the Parabathynellidae and one lineage within the Bathynellidae were found. These lineages did not group within any described genera, and phylogenetic analyses indicated that both local radiations and the retention of a lineage that was more apical in the genealogy account for the diversity within the Parabathynellidae in the Burdekin River alluvial aquifer. Most COI lineages were sampled from only a single bore, although one taxon within the Parabathynellidae was found to be more widespread in the aquifer. Haplotypes within this taxon were not shared among bores (ΦST = 0.603, P < 0.001). Overall, the high species diversity for bathynellaceans from an alluvial aquifer reported here, and surveys of bathynellaceans in several other alluvial systems in south-eastern Australia, suggests that groundwater ecosystems of eastern Australia may contain high stygofaunal diversity by Australian and world standards, particularly at the generic level for parabathynellids.
Additional keywords: Bathynellidae, Burdekin River, cryptic species, connectivity, Parabathynellidae.
References
Abrams, K. M., Guzik, M. T., Cooper, S. J. B., Humphreys, W. F., King, R. A., Cho, J. L., and Austin, A. D. (2012). What lies beneath: molecular phylogenetics and ancestral state reconstruction of the ancient subterranean Australian Parabathynellidae (Syncarida, Crustacea). Molecular Phylogenetics and Evolution 64, 130–144.| What lies beneath: molecular phylogenetics and ancestral state reconstruction of the ancient subterranean Australian Parabathynellidae (Syncarida, Crustacea).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rht1Cnuw%3D%3D&md5=3ad8167df0a1c068bfbc02ff785a060eCAS |
Bentley, A., Schmidt, D., and Hughes, J. M. (2010). Extensive intra-specific genetic diversity of freshwater crayfish in a biodiversity hotspot. Freshwater Biology 55, 1861–1873.
| Extensive intra-specific genetic diversity of freshwater crayfish in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Boulton, A. J. (2009). Recent progress in the conservation of groundwaters and their dependent ecosystems. Aquatic Conservation 19, 731–735.
| Recent progress in the conservation of groundwaters and their dependent ecosystems.Crossref | GoogleScholarGoogle Scholar |
Camacho, A. I., and Hancock, P. (2010a). A new genus of Parabathynellidae (Crustacea: Bathynellacea) in New South Wales, Australia. Journal of Natural History 44, 1081–1094.
| A new genus of Parabathynellidae (Crustacea: Bathynellacea) in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Camacho, A. I., and Hancock, P. (2010b). First record of Syncarida from Queensland, Australia, with description of two new species of Notobathynella Schminke, 1973 (Crustacea, Bathynellacea, Parabathynellidae). Journal of Natural History 45, 113–135.
| First record of Syncarida from Queensland, Australia, with description of two new species of Notobathynella Schminke, 1973 (Crustacea, Bathynellacea, Parabathynellidae).Crossref | GoogleScholarGoogle Scholar |
Camacho, A. I., and Hancock, P. (2012). Two new species of the genus Chilibathynella Noodt, 1963 and Onychobathynella bifurcata gen. et sp. nov (Crustacea: Syncarida: Parabathynellidae) from New South Wales, Australia. Journal of Natural History 46, 145–173.
| Two new species of the genus Chilibathynella Noodt, 1963 and Onychobathynella bifurcata gen. et sp. nov (Crustacea: Syncarida: Parabathynellidae) from New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Chappuis, P.A. (1915). Bathynella natans und ihre Stellung im System. Zoologische Jahrbücher (Systematik, Geographie u. Biologie der Tiere) 40, 147–176.
Cho, J.-L., and Humphreys, W. F. (2010). Ten new species of the genus Brevisomabathynella Cho, Park and Ranga Reddy, 2006 (Malacostraca, Bathynellacea, Parabathynellidae) from Western Australia. Journal of Natural History 44, 993–1079.
| Ten new species of the genus Brevisomabathynella Cho, Park and Ranga Reddy, 2006 (Malacostraca, Bathynellacea, Parabathynellidae) from Western Australia.Crossref | GoogleScholarGoogle Scholar |
Cho, J.-L., Park, J.-G., and Humphreys, W. F. (2005). A new genus and six new species of the Parabathynellidae (Bathynellacea, Syncarida) from the Kimberley region, Western Australia. Journal of Natural History 39, 2225–2255.
| A new genus and six new species of the Parabathynellidae (Bathynellacea, Syncarida) from the Kimberley region, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Cho, J.-L., Humphreys, W. F., and Lee, S.-D. (2006). Phylogenetic relationships within the genus Atopobathynella Schminke (Bathynellacea: Parabathynellidae). Invertebrate Systematics 20, 9–41.
| Phylogenetic relationships within the genus Atopobathynella Schminke (Bathynellacea: Parabathynellidae).Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. (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=6c2fc40b039e7a3121d6b93d4e16a02fCAS |
Cook, B. D., Bunn, S. E., and Hughes, J. M. (2007). A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors? Freshwater Biology 52, 2156–2171.
| A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors?Crossref | GoogleScholarGoogle Scholar |
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 |
Cooper, S. J. B., Saint, K. M., Taiti, S., Austin, A. D., and Humphreys, W. F. (2008). Subterranean archipelago: mitochondrial DNA phylogeography of stygobitic isopods (Oniscidea: Haloniscus) from the Yilgarn region of Western Australia. Invertebrate Systematics 22, 195–203.
| Subterranean archipelago: mitochondrial DNA phylogeography of stygobitic isopods (Oniscidea: Haloniscus) from the Yilgarn region of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Costa, F. O., de Waard, J. R., Boutilier, J., Ratnasingham, S., Dooh, R. T., Hajibabaei, M., and Hebert, P. D. (2007). Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.
| Biological identifications through DNA barcodes: the case of the Crustacea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Gqsbo%3D&md5=c60f8b9f37ee39a574d0b8158e23ff6eCAS |
Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2011). Geneious v5.4. Available from http://www.geneious.com/ [accessed November 2011].
Eberhard, S. E., Halse, S. A., Wiliams, M. R., Scanlon, M. D., Cocking, J., and Barron, H. J. (2009). Exploring the relationship between sampling efficiency and short-range endemism for groundwater fauna in the Pilbara region, Western Australia. Freshwater Biology 54, 885–901.
| Exploring the relationship between sampling efficiency and short-range endemism for groundwater fauna in the Pilbara region, Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVOqurg%3D&md5=5633828a19f28ac19119e6509a40fa3aCAS |
Excoffier, L., and Lischer, H. E. L. (2010). Arelquin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arelquin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |
Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=54b11e3e59d6dd0ba51a273d497b7c25CAS |
Finston, T. L., Johnson, M. S., Humphreys, W. F., Eberhard, S. M., and Halse, S. A. (2007). Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape. Molecular Ecology 16, 355–365.
| Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1yqsrw%3D&md5=34962c05dc921aa155de9ac5948fa5e0CAS |
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=e8bb43588ef5d7ec0926da1a4a680552CAS |
Grobben, K. (1904). ‘Lehrbuch der Zoologie, begrundet von C. Claus, neubearbeitet von Dr Karl Grobben.’ (Publisher unknown: Marburg.)
Guzik, M. T., Abrams, K. M., Cooper, S. J. B., Humphreys, W. F., Cho, J.-L., and Austin, A. D. (2008). Phylogeography of the ancient Parabathynellidae (Crustacea: Bathynellacea) from the Yilgarn region of Western Australia. Invertebrate Systematics 22, 205–216.
| Phylogeography of the ancient Parabathynellidae (Crustacea: Bathynellacea) from the Yilgarn region of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Guzik, M. T., Cooper, S. J. B., Humphreys, C. H. S., and Austin, A. D. (2009). Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia. Molecular Ecology 18, 3683–3698.
| Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WhtrbM&md5=0575a8b268d7e746e09a1b0c01ce6054CAS |
Guzik, M. T., Cooper, S. J. B., Humphrey, W. F., Ong, S., Kawakami, T., and Austin, A. D. (2011a). Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert. Heredity 107, 215–230.
| Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjmslSjtQ%3D%3D&md5=23e7ee903b6818e28aa1668a97d0c027CAS |
Guzik, M. T., Austin, A. D., Cooper, S. J. B., Harvey, M. S., Humphreys, W. F., Bradford, T., Eberhard, S. M., King, R. A., Leys, R., Muirhead, K. A., and Tomlinson, M. (2011b). Is the Australian subterranean fauna uniquely diverse? Invertebrate Systematics 24, 407–418.
| Is the Australian subterranean fauna uniquely diverse?Crossref | GoogleScholarGoogle Scholar |
Hancock, P. J., and Boulton, A. J. (2008). Stygofauna biodiversity and endemism in four alluvial aquifers in eastern Australia. Invertebrate Systematics 22, 117–126.
| Stygofauna biodiversity and endemism in four alluvial aquifers in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Hong, S. J., and Cho, J. L. (2009). Three new species of Billibathynella from Western Australia (Crustacea, Syncarida, Parabathynellidae). Journal of Natural History 43, 2365–2390.
| Three new species of Billibathynella from Western Australia (Crustacea, Syncarida, Parabathynellidae).Crossref | GoogleScholarGoogle Scholar |
Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MrBayes: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=a4aa0a8b9d4b188e002dfccc62355443CAS |
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., Huey, J. A., McLean, A. J., and Baggiano, O. (2011). Aquatic insects in eastern Australia: a window on ecology and evolution of dispersal in streams. Insects 2, 447–461.
| Aquatic insects in eastern Australia: a window on ecology and evolution of dispersal in streams.Crossref | GoogleScholarGoogle Scholar |
Humphreys, W. F. (2008). Rising from Down Under: developments in subterranean biodiversity in Australia from a groundwater fauna perspective. Invertebrate Systematics 22, 85–101.
| Rising from Down Under: developments in subterranean biodiversity in Australia from a groundwater fauna perspective.Crossref | GoogleScholarGoogle Scholar |
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
| A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=07bc4021fc41d46c7a1dcf0e9ec6604eCAS |
Noodt, W. (1965). Natürliches System und Biogeographie der Syncarida (Crustacea Malacostraca). Gewässer und Abwässer 37–38, 77–186.
Page, T.J., Humphreys, W.F., and Hughes, J.M. (2008). Shrimps down under: evolutionary relationships of subterranean crustaceans from Western Australia (Decapoda: Atyidae: Stygiocaris). PLoS ONE 3, e1618.
| Shrimps down under: evolutionary relationships of subterranean crustaceans from Western Australia (Decapoda: Atyidae: Stygiocaris).Crossref | GoogleScholarGoogle Scholar |
Perna, C., O’Connor, R., and Cook, B. (2012). Hydroecology of the Lower Burdekin River Alluvial Aquifer and Associated Groundwater Dependent Ecosystems. Queensland Government, Department of Environment and Resource Management, Brisbane.
Posada, D., and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of the Akaike information criterion and Bayesian approaches over likelihood ration tests. Systematic Biology 53, 793–808.
| Model selection and model averaging in phylogenetics: advantages of the Akaike information criterion and Bayesian approaches over likelihood ration tests.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. J. (2003). ‘Tracer: MCMC Trace Analysis Tool.’ (University of Oxford: Oxford.)
Stamatakis, A., Hoover, P., and Rougmont, J. (2008). A rapid algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
| A rapid algorithm for the RAxML web servers.Crossref | GoogleScholarGoogle Scholar |
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kuma, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=e121185be206a62dd6608c78d1e42defCAS |
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=4f0678b13e5d7904657778cff18d2cf2CAS |
Tomlinson, M., and Boulton, A. J. (2010). Ecology and management of subsurface groundwater dependent ecosystems in Australia – a review. Marine and Freshwater Research 61, 936–949.
| Ecology and management of subsurface groundwater dependent ecosystems in Australia – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVansL7F&md5=cc890215356e185bf0902f038bd8ee29CAS |
