Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Phylogeography of the ancient Parabathynellidae (Crustacea : Bathynellacea) from the Yilgarn region of Western Australia

M. T. Guzik A E , K. M. Abrams A , S. J. B. Cooper A B , W. F. Humphreys C , J.-L. Cho D and A. D. Austin A
+ Author Affiliations
- Author Affiliations

A Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia.

B Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

C Western Australian Museum, Locked Bag 49, Welshpool DC, WA 6986, Australia.

D International Drinking Water Center, San 6-2, Yeonchuck-Dong, Daedok-Gu, Taejeon 306-711, Korea.

E Corresponding author. Email: michelle.guzik@adelaide.edu.au

Invertebrate Systematics 22(2) 205-216 https://doi.org/10.1071/IS07040
Submitted: 30 July 2007  Accepted: 14 February 2008   Published: 12 May 2008

Abstract

The crustacean order Bathynellacea is a primitive group of subterranean aquatic (stygobitic) invertebrates that typically inhabits freshwater interstitial spaces in alluvia. A striking diversity of species from the bathynellacean family Parabathynellidae have been found in the calcretes of the Yilgarn palaeodrainage system in Western Australia. Taxonomic studies show that most species are restricted in their distribution to a single calcrete, which is consistent with the findings of other phylogeographic studies of stygofauna. In this, the first molecular phylogenetic and phylogeographic study of interspecific relationships among parabathynellids, we aimed to explore the hypothesis that species are short-range endemics and restricted to single calcretes, and to investigate whether there were previously unidentified cryptic species. Analyses of sequence data based on a region of the mitochondrial (mt) DNA cytochrome c oxidase 1 gene showed the existence of divergent mtDNA lineages and species restricted in their distribution to a single calcrete, in support of the broader hypothesis that these calcretes are equivalent to closed island habitats comprising endemic taxa. Divergent mtDNA lineages were also observed to comprise four new and 12 recognised morphospecies. These results reflect the findings of previous studies of stygobitic arthropods (beetles, amphipods and isopods) from the Yilgarn region and reinforce the usefulness of using DNA-sequence data to investigate species boundaries and the presence of cryptic species.

Additional keywords: cryptic species, cytochrome c oxidase 1, mitochondrial DNA, phylogeny, stygofauna.


Acknowledgements

The authors would like to thank Peter Hancock for the psammaspid specimen. We also thank R. Leijs, C. Clay, S. Eberhard, H. Hahn, T. Karanovic, S. Hinze, T. Moulds, J. Waldock and C. Watts for help with collection of specimens, and K. Saint and J. Waldock for technical support. This manuscript was greatly improved by the suggestions of three anonymous reviewers, the editor and N. Murphy. This research was supported by an Australian Biological Resources Study grant to MTG and WFH and the Australian Research Council and participating industry partners: Newmont Australia, Placer Dome Asia Pacific, South Australian Museum and Western Australian Museum for a Linkage Grant (LP0348753).


References


Abascal F., Zardoya R., Posada D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Arakel A. V., Jacobson G., Lyons W. B. (1990) Sediment–water interaction as a control on geochemical evolution of playa lake systems in the Australian arid interior. Hydrobiologia 197, 1–12.
Crossref | GoogleScholarGoogle Scholar | open url image1

Avise J. C. (1989) Gene trees and organismal histories: a phylogenetic approach to population biology. Evolution 43, 1192–1208.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beard J. S. (1998) Position and development history of the central watershed of the Western Shield, Western Australia. Journal of the Royal Society of Western Australia 81, 157–164. open url image1

Camacho A. I. (2003) Four new species of groundwater crustaceans (Syncarida, Bathynellacea, Parabathynellidae) endemic to the Iberian Peninsula. Journal of Natural History 37, 2885–2907.
Crossref | GoogleScholarGoogle Scholar | open url image1

Camacho A. I. (2004) An overview of Hexabathynella (Crustacea, Syncarida, Parabathynellidae) with the description of a new species. Journal of Natural History 38, 1249–1261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Camacho A. I. (2006) An annotated checklist of the Syncarida (Crustacea, Malacostraca) of the world. Zootaxa 1374, 1–54. open url image1

Camacho A. I., and Serban E. (1998). Tribu des Iberobathynellini nov., diagnoses des taxa nouveaux (Parabathynellidae, Bathynellacea, Podophallocarida). Travaux de l’Institut de Spéologie ‘Emile Racovitza’ XXXIV, 15–75.

Camacho A. I., Rey I., Dorda B. A., Machordom A., Valdecasas A. G. (2002) A note on the systematic position of the Bathynellacea (Crustacea, Malacostraca) using molecular evidence. Contributions to Zoology 71, 123–129. open url image1

Cho J.-L. (1996) A new species of the genus Texanobathynella from California (Crustacea, Malacostraca, Bathynellacea). Korean Journal of Syststematic Zoology 12, 389–395. open url image1

Cho J.-L. (1997) Two new species of a new genus of Leptobathynellinae (Crustacea, Bathynellacea) from California, USA. Korean Journal of Biological Sciences 1, 265–270. open url image1

Cho J.-L. (2001) Phylogeny and zoogeography of three new species of the genus Hexabathynella (Crustacea, Malacostraca, Bathynellacea) from North America. Zoologica Scripta 30, 145–157.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho J.-L. (2005) A primitive representative of the Parabathynellidae (Bathynellacea, Syncarida) from the Yilgarn Craton of Western Australia. Journal of Natural History 39, 3423–3433.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho J.-L., Schminke H. K. (2001) A revision of the genus Parvulobathynella Schminke, 1973 (Bathynellacea, Parabathynellidae): with the description of two new species from South Africa. Crustaceana 74, 777–796.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho J.-L., Schminke H. K. (2006) A phylogenetic review of the genus Hexabathynella Schminke, 1972 (Crustacea, Malacostraca, Bathynellacea): with a description of four new species. Zoological Journal of the Linnean Society 147, 71–96. open url image1

Cho J.-L., Park J.-G., 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho J.-L., Humphreys W. F., Lee S.-D. (2006a) Phylogenetic relationships within the genus Atopobathynella Schminke (Bathynellacea: Parabathynellidae). Invertebrate Systematics 20, 9–41.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho J.-L., Park J.-G., Reddy Y. R. R. (2006b) Brevisomabathynella gen. nov. with two new species from Western Australia (Bathynellacea, Syncarida): the first definitive evidence of predation in Parabathynellidae. Zootaxa 1247, 25–42. open url image1

Clarke J. D. A. (2001). Ancient landforms of Kambalda and their significance to human activity. In ‘Gondwana to Greenhouse: Australian Environmental Geoscience’. Special Publication 21. (Ed. V. A. Gostin.) pp. 49–57 (Chapter 5). (Geological Society of Australia: Sydney, Australia.)

Coineau N. (2000). Adaptations to interstitial groundwater life. In ‘Ecosystems of the World: Subterranean Ecosystems’. (Eds H. Wilkens, D. C. Culver and W. F. Humphreys.) pp. 189–210. (Elsevier: Amsterdam, The Netherlands.)

Cooper S. J. B., Hinze S., Leys R., Watts C. H. S., Humphreys W. F. (2002) Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera : Dytiscidae) from central Western Australia. Invertebrate Systematics 16, 589–598.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cooper S. J. B., Bradbury J. H., Saint K. M., Leys R., Austin A. D., Humphreys W. F. (2007) Subterranean archipelago in the Australian arid zone: mitochondrial DNA phylogeography of amphipods from central Western Australia. Molecular Ecology 16, 1533–1544.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cooper S. J. B., Saint K. M., Taiti S., Austin A. D., 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Costa F. O., deWaard J. R., Boutillier J., Ratnasingham S., Dooh R. T., Hajibabaei M., Hebert P. D. N. (2007) Biological identifications through barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.
Crossref | GoogleScholarGoogle Scholar | open url image1

Excoffier L., Laval G. and Schneider S. (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.

Finston T. L., Johnson M. S. (2004) Geographic patterns of genetic diversity in subterranean amphipods of the Pilbara, Western Australia. Marine and Freshwater Research 55, 619–628.
Crossref | GoogleScholarGoogle Scholar | open url image1

Finston T. L., Bradbury J. H., Johnson M. S., Knott B. (2004) When morphology and molecular markers conflict: a case history of subterranean amphipods from the Pilbara, Western Australia. Animal Biodiversity and Conservation 27, 83–94. open url image1

Finston T. L., Johnson M. S., Humphreys W. F., Eberhard S. M., 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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Folmer O., Black M., Hoeh W., Lutz R., Vrijenoek R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
PubMed |
open url image1

Fourment M., Gibbs M. J. (2006) PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evolutionary Biology 6, 1.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hajibabaei M., Janzen D. H., Burns J. M., Hallwachs W., Herbert P. D. N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968–971.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hall T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98. open url image1

Huelsenbeck J. P., Ronquist F. (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Humphreys W. F. (2000). Groundwater calcrete aquifers in the Australian arid zone: the context to an unfolding plethora of stygal biodiversity. In ‘Subterranean Biology in Australia 2000’. (Eds W. F. Humphreys and M. S. Harvey.) pp. 63–83. (Western Australian Museum: Perth, Australia.)

Jarman S. N., Elliot N. G. (2000) DNA evidence for morphological and cryptic Cenozoic speciations in the Anaspididae, ‘living fossils’ from the Triassic. Journal of Evolutionary Biology 13, 624–633.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones R., Culver D. C., Kane T. C. (1992) Are parallel morphologies of cave organisms the result of similar selection pressures? Evolution 46, 353–365.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kane T. C., Culver D. C., and Mathieu J. (1994). Biotic fluxes and gene flow. In ‘Groundwater Ecology’. (Eds J. Gibert, D. L. Danielopol and J. Stanford.) pp. 245–259. (Academic Press: New York, USA.)

Karanovic T. (2004). Subterranean copepods (Crustacea : Copepoda) from arid Western Australia. Crustaceana Supplement 70, pp. 1–366.

Kumar S., Tamura K., Nei M. (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lanave C., Preparata G., Saccone C., Serio G. (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution 20, 86–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lefébure T., Douady C. J., Gouy M., Gibert J. (2006a) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lefébure T., Douady C. J., Gouy M., Trontel P., Briolay J., Gibert J. (2006b) Phylogeography of a subterranean amphipod reveals cryptic diversity and dynamic evolution in extreme environments. Molecular Ecology 15, 1797–1806.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leys R., Watts C. H. S., Cooper S. J. B., Humphreys W. F. (2003) Evolution of subterranean diving beetles (Coleoptera : Dytiscidae : Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834.
PubMed |
open url image1

Machida R. J., Miya M. U., Nishida M., Nishida S. (2002) Complete mitochonrial DNA sequence of Tigriopus japonicus (Crustacea : Copepoda). Marine Biotechnology 4, 406–417.
Crossref | PubMed |
open url image1

Mann A. W., Horwitz C. (1979) Groundwater calcrete deposits in Australia: some observations from Western Australia. Journal of the Geological Society of Australia 26, 293–303. open url image1

Moore W. S. (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49, 718–726.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morgan K. H. (1993) Development, sedimentation and economic potential of palaeoriver systems of the Yilgarn Craton of Western Australia. Sedimentary Geology 85, 637–656.
Crossref |
open url image1

Posada D., Crandall K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Proudlove G., Wood P. J. (2003) The blind leading the blind: cryptic subterranean species and DNA taxonomy. Trends in Ecology & Evolution 18, 272–273.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rambaut A., and Drummond A. J. (2003). ‘Tracer: MCMC Trace Analysis Tool.’ University of Oxford, Oxford. http://evolve.zoo.ox. ac.uk/software.html

Ranga Reddy Y. (2002) Habrobathynella nagarjunai n. sp., the second representative of Bathynellacea (Crustacea, Syncarida) from groundwaters of South India. Hydrobiologia 470, 37–43.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ranga Reddy Y. (2006) First Asian report of the genus Chilibathynella Noodt, 1963 (Bathynellacea, Syncarida), with the description and biogeographic significance of a new species from Kotumsar Cave, India. Zootaxa 1370, 23–37. open url image1

Schminke H. K. (1973) Evolution, System und Verbreitungsgeschichte der Familie Parabathynellidae (Bathynellacea, Malacostraca). Akademie der Wissenschaften und der Literatur Mainz, Mathematisch-Naturwissenschaftliche Klasse. Mikrofauna des Meeresbodens 24, 1–192. open url image1

Schminke H. K. (1974) Mesozoic intercontinental relationships as evidenced by bathynellid Crustacea (Syncarida : Malacostraca). Systematic Zoology 23, 157–164.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schminke H. K. (1981) Adaptation of Bathynellacea (Crustacea, Syncarida) to life in the interstitial (“Zoea Theory”). Internationale Revue der Gesamten Hydrobiologie 66, 575–637.
Crossref | GoogleScholarGoogle Scholar | open url image1

Simon C., Frati F., Beckenbach A., Crespi B., Liu H., Flook P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701. open url image1

Stein R., and Robert C. (1986). Siliclastic sediments at sites 588, 590 and 591: Neogene and Paleogene evolution in the southwest Pacific and Australian climate. In ‘Initial Reports of the Deep Sea Drilling Project 90’. pp. 1437–1445. (US Government Printing Office: Washington, DC, USA.)

Swofford D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods).’ (Sinauer Associates: Sunderland, MA, USA.)

Taiti S., and Humphreys W. F. (2001). New aquatic Oniscidea (Crustacea, Isopoda) from groundwater calcretes of Western Australia. In ‘Subterranean Biology in Australia 2000’. (Eds W. F. Humphreys and M. S. Harvey.) pp. 133–151. (Western Australian Museum: Perth, Australia.)

Thompson J. D., Higgins D. G., Gibson T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Valverde J. R., Batuecas B., Moratilla C., Marco R., Garesse R. (1994) The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. Journal of Molecular Evolution 39, 400–408.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Watts C. H. S., Humphreys W. F. (1999) Three new genera and five new species of Dytiscidae (Coleoptera) from underground waters in Australia. Records of the South Australian Museum 32, 121–142. open url image1

Watts C. H. S., Humphreys W. F. (2000) Six new species of Nirridessus and Tjirtudessus (Dytiscidae: Coleoptera) from underground waters in Australia. Records of the South Australian Museum 33, 127–144. open url image1

Watts C. H. S., Humphreys W. F. (2001) A new genus and six new species of Dytiscidae (Coleoptera) from underground waters in the Yilgarn palaeodrainage system of Western Australia. Records of the South Australian Museum 34, 99–114. open url image1

Watts C. H. S., Humphreys W. F. (2003) Twenty-five new Dytiscidae (Coleoptera) of the genera Tjirtudessus Watts & Humphreys, Nirripirti Watts & Humphreys and Bidessodes Regimbart, from underground waters in Australia. Records of the South Australian Museum 36, 135–187. open url image1

Watts C. H. S., Humphreys W. F. (2004) Thirteen new Dytiscidae (Coleoptera) of the genera Boongurrus Larson, Tjirtudessus Watts & Humphreys and Nirripirti Watts and Humphreys, from underground waters in Australia. Transactions of the Royal Society of South Australia 128, 99–129. open url image1

Watts C. H. S., Humphreys W. F. (2006) Twenty-six new Dytiscidae (Coleoptera) of the genera Limbodessus Guignot and Nirripirti Watts & Humphreys, from underground waters in Australia. Transactions of the Royal Society of South Australia 130, 123–185. open url image1

Westheide W. (1987) Progenesis as a principle in meiofauna evolution. Journal of Natural History 21, 843–854.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wilson K., Cahill V., Ballment E., Benzie J. (2000) The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Molecular Biology and Evolution 17, 863–874.
PubMed |
open url image1