Molecular species boundaries in the phreatoicidean genus Amphisopus (Isopoda : Amphisopidae) and evidence for a new freshwater isopod species from Western Australia
Gavin Gouws A B D and Barbara A. Stewart C
+ Author Affiliations
- Author Affiliations
A South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa.
B School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
C Centre of Excellence in Natural Resource Management, The University of Western Australia, PO Box 5771, Albany, WA 6332, Australia.
D Corresponding author. Email: g.gouws@saiab.ac.za
Invertebrate Systematics 27(2) 173-185 https://doi.org/10.1071/IS12043
Submitted: 17 May 2012 Accepted: 8 October 2012 Published: 24 May 2013
Abstract
The freshwater isopod genus Amphisopus is one of only two phreatoicidean genera in Western Australia with wide distributions and containing multiple described species. Two species (Amphisopus annectans and A. lintoni) are known from the south-western part of the state. With recent sampling extending the known range of Amphisopus and the recorded possibility of an undescribed species, this study aimed to examine genetic species boundaries and to detect additional species diversity. Isopods were sampled from across the range, and genetic structure was examined using mtDNA sequence data from a COI fragment and data from ten polymorphic allozyme loci. While allozyme data supported the clear separation of the known species, phylogenetic analyses presented three divergent monophyletic, geographically restricted clades occurring in the western, eastern and central parts of the Amphisopus distribution. These corresponded to A. annectans, A. lintoni and an undescribed species, respectively. The latter’s status was supported by its phylogenetic position relative to the known species and by the extent of differentiation observed among other phreatoicidean taxa. As with other taxa from the region, divergence times among these three species supported aridity in the Miocene–Pliocene as a driver of diversification, and suggested the existence of wetter refugial areas in south-western Australia.
References
Akaike, H. (1974). A new look at the statistical model identification. Institute of Electrical and Electronics Engineers Transactions on Automatic Control 19, 716–723.| A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |
Chilton, C. (1922). A new isopod from central Australia belonging to the Phreatoicidae. Transactions of the Royal Society of South Australia 46, 23–33.
Clarke, J. D. A. (1994). Evolution of Lefroy and Cowan palaeodrainage channels, Western Australia. Australian Journal of Earth Sciences 41, 55–68.
| Evolution of Lefroy and Cowan palaeodrainage channels, Western Australia.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 |
Cooper, S. J. B., Harvey, M. S., Saint, K. M., and Main, B. Y. (2011). Deep phylogeographic structure of the trapdoor spider Moggridgea tingle (Migidae) from southwestern Australia: evidence for long-term refugia within refugia. Molecular Ecology 20, 3219–3236.
| Deep phylogeographic structure of the trapdoor spider Moggridgea tingle (Migidae) from southwestern Australia: evidence for long-term refugia within refugia.Crossref | GoogleScholarGoogle Scholar |
Dodson, J. R., and Macphail, M. K. (2004). Palynological evidence for aridity events and vegetation changes during the Middle Pliocene, a warm period in southwestern Australia. Global and Planetary Change 41, 285–307.
| Palynological evidence for aridity events and vegetation changes during the Middle Pliocene, a warm period in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |
Edward, D. H. D., Gazey, P., and Davies, P. M. (1994). Invertebrate community structure related to physico-chemical parameters of permanent lakes of the south coast of Western Australia. Journal of the Royal Society of Western Australia 77, 51–63.
Edwards, D. L., Roberts, J. D., and Keogh, J. S. (2007). Impact of Plio-Pleistocene arid cycling on the population history of a southwestern Australian frog. Molecular Ecology 16, 2782–2796.
| Impact of Plio-Pleistocene arid cycling on the population history of a southwestern Australian frog.Crossref | GoogleScholarGoogle Scholar | 17594447PubMed |
Edwards, D. L., Roberts, J. D., and Keogh, J. S. (2008). Climatic fluctuations shape the phylogeography of a mesic direct-developing frog from the south-western Australian biodiversity hotspot. Journal of Biogeography 35, 1803–1815.
| Climatic fluctuations shape the phylogeography of a mesic direct-developing frog from the south-western Australian biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |
Excoffier, L., Smouse, P., and Quattro, J. (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=464435ff2610f84a09c1af7039f22f27CAS | 1644282PubMed |
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Felsenstein, J. (2002). ‘PHYLIP (Phylogeny Inference Package), version 3.6a3.’ (Department of Genome Sciences, University of Washington: Seattle, WA, USA.)
Finston, T. L., Francis, C. J., and Johnson, M. S. (2009). Biogeography of the stygobitic isopod Pygolabis (Malacostraca: Tainisopidae) in the Pilbara, Western Australia: evidence for multiple colonisations of the groundwater. Molecular Phylogenetics and Evolution 52, 448–460.
| Biogeography of the stygobitic isopod Pygolabis (Malacostraca: Tainisopidae) in the Pilbara, Western Australia: evidence for multiple colonisations of the groundwater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12hsbs%3D&md5=b32d7c30dd1d206b4ec0ac390ed5648fCAS | 19303454PubMed |
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=5041ee59b321d3be53c601c4defe3469CAS | 7881515PubMed |
Glauert, L. (1924). Contributions to the fauna of Western Australia, no. 4. A freshwater isopod Phreatoicus palustris. n. sp. Journal of the Royal Society of Western Australia 10, 49–57.
Gouws, G. (2008). New species of Mesamphisopus, an endemic South African freshwater isopod genus (Isopoda: Phreatoicidea: Mesamphisopidae). Zootaxa 1690, 1–62.
Gouws, G., and Stewart, B. A. (2007). From genetic structure to wetland conservation: a freshwater isopod Paramphisopus palustris (Phreatoicidea: Amphisopidae) from the Swan Coastal Plain, Western Australia. Hydrobiologia 589, 249–263.
| From genetic structure to wetland conservation: a freshwater isopod Paramphisopus palustris (Phreatoicidea: Amphisopidae) from the Swan Coastal Plain, Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotVaguro%3D&md5=5e6830aaff66a8859c8fce76c726d9baCAS |
Gouws, G., Stewart, B. A., and Daniels, S. R. (2004). Cryptic species within the freshwater isopod Mesamphisopus capensis (Phreatoicidea: Amphisopodidae) in the Western Cape, South Africa: allozyme, 12S rRNA sequence data and morphometric evidence. Biological Journal of the Linnean Society. Linnean Society of London 81, 235–253.
| Cryptic species within the freshwater isopod Mesamphisopus capensis (Phreatoicidea: Amphisopodidae) in the Western Cape, South Africa: allozyme, 12S rRNA sequence data and morphometric evidence.Crossref | GoogleScholarGoogle Scholar |
Gouws, G., Stewart, B. A., and Matthee, C. A. (2005). Lack of taxonomic differentiation in an apparently widespread freshwater isopod morphotype (Phreatoicidea: Mesamphisopidae: Mesamphisopus) from South Africa. Molecular Phylogenetics and Evolution 37, 289–305.
| Lack of taxonomic differentiation in an apparently widespread freshwater isopod morphotype (Phreatoicidea: Mesamphisopidae: Mesamphisopus) from South Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVart7nO&md5=325073ac7ed5316fe6479152e5e290b0CAS | 16111899PubMed |
Gouws, G., Stewart, B. A., and Daniels, S. R. (2006). Phylogeographic structure of a freshwater crayfish (Decapoda: Parastacidae: Cherax preissii) in south-western Australia. Marine and Freshwater Research 57, 837–848.
| Phylogeographic structure of a freshwater crayfish (Decapoda: Parastacidae: Cherax preissii) in south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OgsLfI&md5=bfcd0739336dd4558089cee9316f5629CAS |
Gouws, G., Matthee, C. A., and Stewart, B. A. (2010a). A multiple data set phylogeny for the endemic South African freshwater phreatoicidean isopod genus Mesamphisopus: taxonomic and biogeographic implications. Molecular Phylogenetics and Evolution 55, 541–551.
| A multiple data set phylogeny for the endemic South African freshwater phreatoicidean isopod genus Mesamphisopus: taxonomic and biogeographic implications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3jt1aquw%3D%3D&md5=54aaa7e5d820e432b539979f49419098CAS | 20096796PubMed |
Gouws, G., Stewart, B. A., and Daniels, S. R. (2010b). Phylogeographic structure in the gilgie (Decapoda: Parastacidae: Cherax quinquecarinatus): a south-western Australian freshwater crayfish. Biological Journal of the Linnean Society. Linnean Society of London 101, 385–402.
| Phylogeographic structure in the gilgie (Decapoda: Parastacidae: Cherax quinquecarinatus): a south-western Australian freshwater crayfish.Crossref | GoogleScholarGoogle Scholar |
Harris, P., Heap, A., Passlow, V., Sbaffi, L., Fellows, M., Porter-Smith, R., Buchanan, C., and Daniell, J. (2005). ‘Geomorphic Features of the Continental Margin of Australia. Record 2003/30.’ (Geoscience Australia: Canberra, Australia.)
Hopper, S. D., and Goia, P. (2004). The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology Evolution and Systematics 35, 623–650.
| The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity.Crossref | GoogleScholarGoogle Scholar |
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=9c2a21396720b47f0b5ec58cc9c74affCAS | 12535105PubMed |
Knott, B., and Halse, S. A. (1999). Pilbarophreatoicus platyarthricus n.gen., n.sp. (Isopoda: Phreatoicidea: Amphisopodidae) from the Pilbara Region of Western Australia. Records of the Australian Museum 51, 33–42.
| Pilbarophreatoicus platyarthricus n.gen., n.sp. (Isopoda: Phreatoicidea: Amphisopodidae) from the Pilbara Region of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for molecular genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| MEGA3: integrated software for molecular genetics analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=2e07832f47b10f2d3caf2c47844be434CAS | 15260895PubMed |
Nei, M. (1978). Estimates of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
| 1:STN:280:DC%2BC3crpt1Kqtg%3D%3D&md5=772287cd29d5c74da1245dca8847c805CAS | 17248844PubMed |
Nicholls, G. E. (1924). Phreatoicus lintoni, a new species of freshwater isopod from south-western Australia. Journal of the Royal Society of Western Australia 10, 91–103.
Nicholls, G. E. (1926). A description of two new genera and species of Phreatoicidea, with a discussion of the affinities of the members of this family. Journal of the Royal Society of Western Australia 12, 179–209.
Nicholls, G. E. (1943). The Phreatoicoidea. Part I. The Amphisopidae. Papers and Proceedings of the Royal Society of Tasmania 1942, 1–145.
Nicholls, G. E., and Milner, D. F. (1923). A new genus of fresh-water isopod, allied to Phreatoicus. Journal of the Royal Society of Western Australia 10, 23–34.
Poore, G. C. B., and Humphreys, W. F. (1998). First record of Spelaeogriphacea from Australasia: a new genus and species from an aquifer in the arid Pilbara of Western Australia. Crustaceana 71, 721–742.
| First record of Spelaeogriphacea from Australasia: a new genus and species from an aquifer in the arid Pilbara of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Posada, D., and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| MODELTEST: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=ecf9443a01ac004cd72c636453c30354CAS | 9918953PubMed |
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
| Analyzing tables of statistical tests.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=c60b5f7b2a55d284223f3a076ea93fe5CAS | 12912839PubMed |
Schultz, M. B., Ierodiaconou, D. A., Smith, S. A., Horwitz, P., Richardson, A. M. M., Crandall, K. A., and Austin, C. M. (2008). Sea-level changes and palaeo-ranges: reconstruction of ancient shorelines and river drainages and the phylogeography of the Australian land crayfish Engaeus sericatus Clark (Decapoda: Parastacidae). Molecular Ecology 17, 5291–5314.
| Sea-level changes and palaeo-ranges: reconstruction of ancient shorelines and river drainages and the phylogeography of the Australian land crayfish Engaeus sericatus Clark (Decapoda: Parastacidae).Crossref | GoogleScholarGoogle Scholar | 19120999PubMed |
Sheppard, E. M. (1927). Revision of the family Phreatoicidae (Crustacea), with a description of two new species. Proceedings of the Royal Society of London 1927, 81–124.
Shimodaira, H., and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.
| Multiple comparisons of log-likelihoods with applications to phylogenetic inference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVyksrg%3D&md5=4216a5b088526016a3d94091cd1e46b0CAS |
Smith, M. J., Kay, W. R., Edward, D. H. D., Papas, P. J., Richardson, K. St. J., Simpson, J. C., Pinder, A. M., Cale, D. J., Horwitz, P. H. J., Davis, J. A., Yung, F. H., Norris, R. H., and Halse, S. A. (1999). AusRivAS: using macroinvertebrates to assess ecological conditions of rivers in Western Australia. Freshwater Biology 41, 269–282.
| AusRivAS: using macroinvertebrates to assess ecological conditions of rivers in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Sneath, P. H. A., and Sokal, R. R. (1973). ‘Numerical Taxonomy: the Principles and Practice of Numerical Classification.’ (W. H. Freeman and Company: San Francisco, CA, USA.)
Stephens, J. C., and Nei, M. (1985). Phylogenetic analysis of polymorphic DNA sequences at the Adh locus in Drosophila melanogaster and its sibling species. Journal of Molecular Evolution 22, 289–300.
| Phylogenetic analysis of polymorphic DNA sequences at the Adh locus in Drosophila melanogaster and its sibling species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xmtlalsg%3D%3D&md5=b4a3c7c0d32cdc66a59c5c2172e65b6aCAS | 3003368PubMed |
Stewart, B. A., Gouws, G., Daniels, S. R., and Matthee, C. A. (2004). Delimitation of morphologically similar sponge crab species of the genus Pseudodromia (Crustacea: Decapoda: Dromiidae) from South Africa. Zoologica Scripta 33, 45–55.
| Delimitation of morphologically similar sponge crab species of the genus Pseudodromia (Crustacea: Decapoda: Dromiidae) from South Africa.Crossref | GoogleScholarGoogle Scholar |
Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.’ (Sinauer Associates Inc.: Sunderland, MA, USA.)
Swofford, D. L., Selander, R. B., and Black, W. C. (1997). ‘BIOSYS-2: A Computer Program for the Analysis of Allelic Variation in Genetics.’ (Department of Genetics and Development, University of Illinois at Urbana-Champaign: Urbana, IL, USA.)
Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.
| 1:CAS:528:DyaK3sXks1CksL4%3D&md5=bd12ce159ae61319504eda35a645916cCAS | 8336541PubMed |
Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. In ‘Some Mathematical Questions in Biology – DNA Sequence Analysis’. (Ed. R. M. Miura.) pp. 57–86. (American Mathematical Society: Providence, RI, USA.)
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The ClustalX windows interface. flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The ClustalX windows interface. flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=b8cf08dce6fdc7c2e66332a68e4a4aa4CAS | 9396791PubMed |
Unmack, P. J. (2001). Biogeography of Australian freshwater fishes. Journal of Biogeography 28, 1053–1089.
| Biogeography of Australian freshwater fishes.Crossref | GoogleScholarGoogle Scholar |
Walsh, P. S., Metzger, D. A., and Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513.
| 1:STN:280:DyaK3MzivFSjtw%3D%3D&md5=dbd9d01f1982f087f0356f2a5787ad92CAS | 1867860PubMed |
Wilson, G. D. F. (2003). A new genus of Tainisopidae fam. nov. (Crustacea: Isopoda) from the Pilbara, Western Australia. Zootaxa 245, 1–20.
Wilson, G. D. F. (2008). Global diversity of isopod crustaceans (Crustacea; Isopoda) in freshwater. Hydrobiologia 595, 231–240.
| Global diversity of isopod crustaceans (Crustacea; Isopoda) in freshwater.Crossref | GoogleScholarGoogle Scholar |
Wilson, G. D. F., and Edgecombe, G. D. (2003). The Triassic isopod Protamphisopus wianamattensis (Chilton) and comparison with extant taxa (Crustacea, Phreatoicidea). Journal of Paleontology 77, 454–470.
| The Triassic isopod Protamphisopus wianamattensis (Chilton) and comparison with extant taxa (Crustacea, Phreatoicidea).Crossref | GoogleScholarGoogle Scholar |
Wilson, G. D. F., and Johnson, R. T. (1999). Ancient endemism among freshwater isopods (Crustacea, Phreatoicidea). In ‘The Other 99%. The Conservation and Biodiversity of Invertebrates’. (Eds W. Ponder, and D. Lunney.) pp. 264–268. (Transactions of the Royal Zoological Society of New South Wales: Sydney, Australia.)
Wilson, G. D. F., and Keable, S. J. (1999). A new genus of phreatoicidean isopod (Crustacea) from the north Kimberley region, Western Australia. Zoological Journal of the Linnean Society 126, 51–79.
| A new genus of phreatoicidean isopod (Crustacea) from the north Kimberley region, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Wilson, G. D. F., and Keable, S. J. (2001). Systematics of the Phreatoicidea. In ‘Isopod Systematics and Evolution. Crustacean Issues 13’. (Eds B. Kensley, and R. C. Brusca.) pp. 175–194. (A. A. Balkema: Rotterdam, Netherlands.)
Wilson, G. D. F., and Keable, S. J. (2002a). New genera of Phreatoicidea (Crustacea: Isopoda) from Western Australia. Records of the Australian Museum 54, 41–70.
| New genera of Phreatoicidea (Crustacea: Isopoda) from Western Australia.Crossref | GoogleScholarGoogle Scholar |
Wilson, G. D. F., and Keable, S. J. (2002b). New Phreatoicidea (Crustacea: Isopoda) from Grampians National Park, with revisions of Synamphisopus and Phreatoicopsis. Memoirs Museum Victoria 59, 457–529.
Wilson, G. D. F., and Keable, S. J. (2004). A new family and genus of Phreatoicidea (Crustacea: Isopoda) from artesian springs in southwestern Queensland, Australia. Memoirs of the Queensland Museum 49, 741–759.
Wilson, G. D. F., and Ponder, W. F. (1992). Extraordinary new subterranean isopods (Peracarida: Crustacea) from the Kimberley Region, Western Australia. Records of the Australian Museum 44, 279–298.
| Extraordinary new subterranean isopods (Peracarida: Crustacea) from the Kimberley Region, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Wilson, G. D. F., Humphrey, C. L., Colgan, D. J., Gray, K.-A., and Johnson, R. N. (2009). Monsoon-influenced speciation patterns in a species flock of Eophreatiocus Nicholls (Isopoda; Crustacea). Molecular Phylogenetics and Evolution 51, 349–364.
| Monsoon-influenced speciation patterns in a species flock of Eophreatiocus Nicholls (Isopoda; Crustacea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFemur0%3D&md5=702ff8e2b8eaf6e6b76a193c9d5520baCAS |
