Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

A molecular assessment of species boundaries and phylogenetic affinities in Mogurnda (Eleotridae): a case study of cryptic biodiversity in the Australian freshwater fishes

Mark Adams A B E , Timothy J. Page C , David A. Hurwood C D and Jane M. Hughes C
+ Author Affiliations
- Author Affiliations

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

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

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

D Science and Engineering Faculty, Queensland University of Technology, Brisbane, Qld 4000, Australia.

E Corresponding author. Email: mark.adams@samuseum.sa.gov.au

Marine and Freshwater Research 64(10) 920-931 https://doi.org/10.1071/MF12237
Submitted: 29 August 2012  Accepted: 2 April 2013   Published: 21 June 2013

Abstract

As the driest inhabitable continent, it comes as no surprise that Australia has comparatively few species of freshwater-dependent fishes compared with land masses of similar size and latitudinal coverage. In addition to relatively low rainfall and few permanent waterbodies, a range of other climatic, geological, physical, and biogeographical factors are generally offered up, to account for the low species count in a country otherwise regarded as mega-biodiverse. Here, we challenge this traditional view by hypothesising that Australia’s lack of freshwater fishes largely reflects a dearth of detailed taxonomic activity. Using both allozyme and mtDNA markers, we undertook a molecular assessment on the Australian purple-spotted gudgeons (Mogurnda), recently subjected to a taxonomic revision that saw a three-fold increase in the number of described species. In addition to demonstrating additional, species-level biodiversity within M. adspersa, our genetic data revealed discordant patterns of mitochondrial and nuclear genetic affinities among populations in several species, plus a sister relationship between the two central Australian species. We discuss the broader implications of such cryptic biodiversity for the Australian freshwater fish fauna; most notable among these is our prediction that only 50% of species have been described.

Additional keywords: cryptic species, M. mogurnda, molecular systematics, phylogeography, taxonomic impediment, US fishes.


References

Adams, M., Wedderburn, S. D., Unmack, P. J., Hammer, M. P., and Johnson, J. B. (2011). Congeneric assessment demonstrates the linked genetic histories of two threatened fishes (Atherinidae: Craterocephalus) in Australia’s Murray–Darling Basin. Conservation Biology 25, 767–776.
Congeneric assessment demonstrates the linked genetic histories of two threatened fishes (Atherinidae: Craterocephalus) in Australia’s Murray–Darling Basin.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MfgsVWnsQ%3D%3D&md5=faf60d292944f78b1526d10999e14a6eCAS | 21676026PubMed |

Allen, G. R. (1989). ‘Freshwater Fishes of Australia.’ (T. F. H. Publications: Neptune City, NJ.)

Allen, G. R. (1991). ‘Field Guide to the Freshwater Fishes of New Guinea.’ (Christensen Research Institute: Madang, Papua New Guinea.)

Allen, G. R., and Jenkins, A. P. (1999). A review of the Australian freshwater gudgeon, genus Mogurnda (Eleotridae) with descriptions of three new species. Aqua Journal of Ichthyology and Aquatic Biology 3, 141–156.

Allen, G. R., Midgley, S. H., and Allen, M. (2002). ‘Field Guide to the Freshwater Fishes of Australia.’ (Western Australian Museum: Perth.)

Ayala, F. J., and Powell, J. R. (1972). Allozymes as diagnostic characters of sibling species of Drosophila. Proceedings of the National Academy of Sciences, USA 69, 1094–1096.
Allozymes as diagnostic characters of sibling species of Drosophila.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE383ht1Kisw%3D%3D&md5=d7cc84a2bdd789bef2b753c9c1b1149cCAS |

Beheregaray, L. B., and Caccone, A. (2007). Cryptic biodiversity in a changing world. Journal of Biology 6, 9.1–9.5.
Cryptic biodiversity in a changing world.Crossref | GoogleScholarGoogle Scholar |

Bertozzi, T., Adams, M., and Walker, K. F. (2000). Species boundaries in carp gudgeons (Eleotrididae: Hypseleotris) from the River Murray, South Australia: evidence for multiple species and extensive hybridization. Marine and Freshwater Research 51, 805–815.
Species boundaries in carp gudgeons (Eleotrididae: Hypseleotris) from the River Murray, South Australia: evidence for multiple species and extensive hybridization.Crossref | GoogleScholarGoogle Scholar |

Bostock, B. M., Adams, M., Laurenson, L. J. B., and Austin, C. M. (2006). The molecular systematics of Leiopotherapon unicolor (Gunther, 1859): testing for cryptic speciation in Australia’s most widespread freshwater fish. Biological Journal of the Linnean Society. Linnean Society of London 87, 537–552.
The molecular systematics of Leiopotherapon unicolor (Gunther, 1859): testing for cryptic speciation in Australia’s most widespread freshwater fish.Crossref | GoogleScholarGoogle Scholar |

Chapman, A. D. (2005). ‘Numbers of Living Species in Australia and the World.’ (Australian Biological Resources Study: Canberra.)

Cook, B. D., Kennard, M., Real, K., Pusey, B. J., and Hughes, J. M. (2011). Landscape genetic analysis of the tropical freshwater fish Mogurnda mogurnda (Eleotridae) in a monsoonal river basin: importance of hydrographic factors and population history. Freshwater Biology 56, 812–827.
Landscape genetic analysis of the tropical freshwater fish Mogurnda mogurnda (Eleotridae) in a monsoonal river basin: importance of hydrographic factors and population history.Crossref | GoogleScholarGoogle Scholar |

Doyle, J. J., and Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19, 11–15.

Dudgeon, D., Arthington, A. H., Gessner, M. O., Kawabata, Z.-I., Knowler, D. J., Lévêque, C., Naiman, R. J., Prieur-Richard, A., Soto, D., Stiassny, M. L. J., and Sullivan, C. A. (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews of the Cambridge Philosophical Society 81, 163–182.
Freshwater biodiversity: importance, threats, status and conservation challenges.Crossref | GoogleScholarGoogle Scholar | 16336747PubMed |

Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19.
Is a new and general theory of molecular systematics emerging?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVKgtbs%3D&md5=5132c3c38828901ecb993606dcacfd52CAS | 19146594PubMed |

Faulks, L. K., Gilligan, D. M., and Beheregaray, L. B. (2008). Phylogeography of a threatened freshwater fish (Mogurnda adspersa) in eastern Australia: conservation implications. Marine and Freshwater Research 59, 89–96.
Phylogeography of a threatened freshwater fish (Mogurnda adspersa) in eastern Australia: conservation implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKntL8%3D&md5=417ca97e250484782cc52da7ab2a9002CAS |

Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington: Seattle, WA.

Glover, C. J. M. (1989). Fishes. In ‘Natural History of Dalhousie Springs’. (Eds W. Zeidler and W. F. Ponder.) pp. 89–112. (South Australian Museum: Adelaide.)

Guindon, S., and Gascuel, O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |

Hammer, M. P., Adams, M., and Hughes, J. M. (2013). Evolutionary processes and biodiversity. In ‘Ecology of Australian Freshwater Fishes’. (Eds K. Walker and P. Humphreys.) pp. 49–79. (CSIRO Publishing: Melbourne.)

Hammer, M. P., Adams, M., Unmack, P. J., and Walker, K. F. (2007). A rethink on Retropinna: conservation implications of new taxa and significant genetic substructure in Australian smelts (Pisces: Retropinnidae). Marine and Freshwater Research 58, 327–341.
A rethink on Retropinna: conservation implications of new taxa and significant genetic substructure in Australian smelts (Pisces: Retropinnidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1entbY%3D&md5=a17f8d3122845d5619fba708be4d9e82CAS |

Herbert, B., and Peeters, J. (1995). ‘Freshwater Fishes of Far North Queensland.’ (Queensland Department of Primary Industries: Brisbane.)

Hoese, D. F., Larson, H. K., and Llewellyn, L. C. (1980). Family Eleotridae gudgeons. In ‘Freshwater Fishes of South-eastern Australia’. (Ed. R. M. McDowall.) pp. 169–185. (Reed Books: Sydney.)

Hoese, D. F., Bray, D. J., Allen, G. R., Paxton, J. R., Wells, A., and Beesley, P. L. (2007). ‘Zoological Catalogue of Australia, Vol. 35, Parts 1–3. Fishes.’ (CSIRO Publishing/Australian Biological Resources Study: Melbourne.)

Horner, P., and Adams, M. (2007). A molecular systematic assessment of species boundaries in Australian Cryptoblepharus (Reptilia: Squamata: Scincidae) – a case study for the combined use of allozymes and morphology to explore cryptic biodiversity. The Beagle. Records of the Museums and Art Galleries of the Northern Territory , 1–19.

Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=9ad0189a867c8d19f8012b0a092c542dCAS | 11524383PubMed |

Hughes, J. M., Real, K. M., Marshall, J. C., and Schmidt, D. J. (2012). Extreme genetic structure in a small-bodied freshwater fish, the purple spotted gudgeon, Mogurnda adspersa (Eleotridae). PLoS ONE 7, e40546.
Extreme genetic structure in a small-bodied freshwater fish, the purple spotted gudgeon, Mogurnda adspersa (Eleotridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOnsL3M&md5=541d331e918694a2138ea39fd203163aCAS | 22808190PubMed |

Hurwood, D. A., and Hughes, J. M. (1998). Phylogeography of the freshwater fish, Mogurnda adspersa, in streams of northeastern Queensland, Australia: evidence for altered drainage patterns. Molecular Ecology 7, 1507–1517.
Phylogeography of the freshwater fish, Mogurnda adspersa, in streams of northeastern Queensland, Australia: evidence for altered drainage patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFSgtL8%3D&md5=e309b33120e3fc9962f6e1efbdcdb0e5CAS | 9819905PubMed |

Leis, J., Gomon, M., and Larson, H. (2007). Australian fish taxonomists – an endangered species. Australian Society for Fish Biology Newsletter 37, 8–11.

Lundberg, J. G., Kottelat, M., Smith, G. R., Stiassny, M. L. J., and Gill, A. C. (2000). So many fishes, so little time: an overview of recent ichthyological discovery in continental waters. Annals of the Missouri Botanical Garden 87, 26–62.
So many fishes, so little time: an overview of recent ichthyological discovery in continental waters.Crossref | GoogleScholarGoogle Scholar |

Merrick, J. R., and Schmida, G. E. (1984). ‘Australian Freshwater Fishes, Biology and Management.’ (Griffin Press: Adelaide.)

Meyer, A. (1994). Shortcomings of the Cytochrome b gene as a molecular marker. Trends in Ecology & Evolution 9, 278–280.
Shortcomings of the Cytochrome b gene as a molecular marker.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFSkuw%3D%3D&md5=f33eaf3a1198b72170b5ac7ae7b2f228CAS |

Miya, M., Takeshima, H., Endo, H., Ishiguro, N. B., Inoue, J. G., Mukai, T., Satoh, T. P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K., Shirai, S. M., and Nishida, M. (2003). Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 26, 121–138.
Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1WhtL4%3D&md5=f11058b7486572bce108a34ce7af4dfcCAS | 12470944PubMed |

Morris, S. A., Pollard, D. A., Gehrke, P. C., and Pogonoski, J. J. (2001). Threatened and potentially threatened freshwater fishes of coastal New South Wales and the Murray–Darling Basin. New South Wales Fisheries, Sydney.

O’Connor, D., and Moritz, C. (2003). A molecular phylogeny of the Australian skink genera Eulamprus, Gnypetoscincus and Nangura. Australian Journal of Zoology 51, 317–330.
A molecular phylogeny of the Australian skink genera Eulamprus, Gnypetoscincus and Nangura.Crossref | GoogleScholarGoogle Scholar |

Olden, J. D., and Kennard, M. J. (2010). Intercontinental comparison of fish life history strategies along a gradient of hydrologic variability. American Fisheries Society Symposium 73, 83–107.

OZCAM (2012). ‘Online Zoological Collections of Australian Museums.’ Available at http://ozcam.ala.org.au/ [Accessed 17 August 2012].

Page, L. M., and Burr, B. M. (1991). ‘A Field Guide to Freshwater Fishes (North America north of Mexico).’ (Houghton Mifflin Company: Boston, MA.)

Page, T. J., and Hughes, J. M. (2010). Comparing the performance of multiple mitochondrial genes in the analysis of Australian freshwater fishes. Journal of Fish Biology 77, 2093–2122.
Comparing the performance of multiple mitochondrial genes in the analysis of Australian freshwater fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKitrs%3D&md5=3e8912c45caa51f1e995c3a44ec45c10CAS | 21133918PubMed |

Page, T. J., Marshall, J. C., and Hughes, J. M. (2012). The world in a grain of sand: evolutionarily relevant, small-scale freshwater bioregions on sub-tropical dune islands. Freshwater Biology 57, 612–627.
The world in a grain of sand: evolutionarily relevant, small-scale freshwater bioregions on sub-tropical dune islands.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=9ca7868daba5deea747ffd816456e78eCAS | 9918953PubMed |

Poss, S. G., and Collette, B. B. (1995). Second survey of fish collections in the United States and Canada. Copeia 1995, 48–70.
Second survey of fish collections in the United States and Canada.Crossref | GoogleScholarGoogle Scholar |

Pusey, B. J., and Kennard, M. J. (1996). Species richness and geographical variation in assemblage structure of the freshwater fish fauna of the wet tropics region of northern Queensland. Marine and Freshwater Research 47, 563–573.
Species richness and geographical variation in assemblage structure of the freshwater fish fauna of the wet tropics region of northern Queensland.Crossref | GoogleScholarGoogle Scholar |

Pusey, B., Kennard, M., and Arthington, A. (2004). ‘Freshwater Fishes of North-eastern Queensland.’ (CSIRO Publishing: Melbourne.)

Raadik, T. A. (2011). Systematic revision of the mountain galaxias, Galaxias olidus Günther, 1866 species complex (Pisces: Galaxiidae) in eastern Australia. Ph.D. Thesis, University of Canberra.

Raymond, M., and Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.

Richardson, B. J., Baverstock, P. R., and Adams, M. (1986). ‘Allozyme Electrophoresis: a Handbook for Animal Systematics and Population Studies.’ (Academic Press: Sydney.)

Schneider, C. J., Cunningham, M., and Moritz, C. (1998). Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia. Molecular Ecology 7, 487–498.
Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia.Crossref | GoogleScholarGoogle Scholar |

Schönhuth, S., Hillis, D. M., Neely, D. A., Lozano-Vilano, L., Perdices, A., and Mayden, R. L. (2012). Phylogeny, diversity, and species delimitation of the North American round-nosed minnows (Teleostei: Dionda), as inferred from mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 62, 427–446.
Phylogeny, diversity, and species delimitation of the North American round-nosed minnows (Teleostei: Dionda), as inferred from mitochondrial and nuclear DNA sequences.Crossref | GoogleScholarGoogle Scholar | 22056492PubMed |

Swofford, D. L. (2002). ‘PAUP* Version 4.0b5. Phylogenetic Analysis Using Parsimony (*and other methods).’ (Sinauer Associates: Sunderland, MA.)

Unmack, P. J. (2001). Biogeography of Australian freshwater fishes. Journal of Biogeography 28, 1053–1089.
Biogeography of Australian freshwater fishes.Crossref | GoogleScholarGoogle Scholar |

Unmack, P. J. (2013). Biogeography. In ‘Ecology of Australian Freshwater Fishes’. (Eds K. Walker and P. Humphreys.) pp. 25–48. (CSIRO Publishing: Melbourne.)

Vörösmarty, C. J., McIntyre, P. B., Gessner, M. O., Dudgeon, D., Prusevich, A., Green, P., Glidden, S., Bunn, S. E., Sullivan, C. A., Reidy Liermann, C., and Davies, P. M. (2010). Global threats to human water security and river biodiversity. Nature 467, 555–561.
Global threats to human water security and river biodiversity.Crossref | GoogleScholarGoogle Scholar | 20882010PubMed |

Ward, R. D., Hanner, R., and Hebert, P. D. N. (2009). The campaign to DNA barcode all fishes, FISH-BOL. Journal of Fish Biology 74, 329–356.
The campaign to DNA barcode all fishes, FISH-BOL.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvVWrsbw%3D&md5=1a84682474245154328395016c9c5f5bCAS | 20735564PubMed |

Williams, W. D., and Allen, G. R. (1987). Origins and adaptations of the fauna of inland waters. In ‘Fauna of Australia’. (Ed. G. R. Dyne.) pp. 184–201. (Australian Government Printing Service: Canberra.)

Williams, J., Read, C., Norton, A., Dovers, S., Burgman, M., Proctor, W., and Anderson, H. (2001). ‘Biodiversity, Australia State of the Environment Report 2001 (Theme Report), Department of the Environment and Heritage.’ (CSIRO Publishing: Melbourne.)

Zardoya, R., and Meyer, A. (1996). Phylogenetic performance of mitochondrial protein coding genes in resolving relationships among vertebrates. Molecular Biology and Evolution 13, 933–942.
Phylogenetic performance of mitochondrial protein coding genes in resolving relationships among vertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlSmsLo%3D&md5=4d4600086912b72e16073c4a2567b9ebCAS | 8752002PubMed |