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Advances in the aquatic sciences
RESEARCH ARTICLE

Phylogeography of two freshwater prawn species from far-northern Queensland

Sofie J. Bernays A C , Daniel J. Schmidt A , David A. Hurwood B and Jane M. Hughes A
+ Author Affiliations
- Author Affiliations

A Australian Rivers Institute, Griffith University, 170 Kessels Road, Nathan, Qld 4111, Australia.

B Earth, Environmental and Biological Sciences, Queensland University of Technology, 2 George Street, Gardens Point, Qld 4000, Australia.

C Corresonding author. Email: sofie.bernays@griffithuni.edu.au

Marine and Freshwater Research 66(3) 256-266 https://doi.org/10.1071/MF14124
Submitted: 8 May 2014  Accepted: 17 July 2014   Published: 5 November 2014

Abstract

The distribution of a freshwater species is often dependent on its ability to disperse within the riverine system. Species with high dispersal abilities tend to be widespread, whereas those with restricted dispersal tend to be geographically restricted and are usually given higher conservation priority. Population structure was compared between a widespread freshwater prawn species, Macrobrachium australiense, and a narrow-range endemic freshwater prawn, Macrobrachium koombooloomba. The distribution of M. australiense and M. koombooloomba did not overlap, although suggested historical river-boundary rearrangements indicate that there has been the potential for dispersal into neighbouring catchments. A fragment of the mtDNA CO1 gene was analysed and a Mantel test revealed a significant isolation by distance effect for both species. Significant overall FST values confirmed that both species exhibited low levels of dispersal, a prediction for populations inhabiting a fragmented upland environment. The level of structure in M. australiense is surprising for a widely distributed species. Not all M. australiense populations conformed to the stream-hierarchy model, with results being best explained by historical river realignment or cross-catchment dispersal. The fact that both species show limited dispersal highlights the importance of conservation in highland areas for both endemic and widely spread species.

Additional keywords: Atherton Tablelands, COI, historical river realignment, Macrobrachium koombooloomba, Macrobrachium australiense, mtDNA, population structure, short-range endemic, shrimp, upland, widely distributed.


References

Alp, M., Keller, I., Westram, A. M., and Robinson, C. T. (2012). How river structure and biological traits influence gene flow: a population genetic study of two stream invertebrates with differing dispersal abilities. Freshwater Biology 57, 969–981.
How river structure and biological traits influence gene flow: a population genetic study of two stream invertebrates with differing dispersal abilities.Crossref | GoogleScholarGoogle Scholar |

Benson, D., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D., Ostell, J., and Sayers, E. (2013). GenBank. Nucleic Acids Research 41, D36–D42.
GenBank.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ksbjJ&md5=fc89d7e4af4a33af8e44f8266d421dceCAS | 23193287PubMed |

Bishop, P. (1995). Drainage rearrangement by river capture, beheading and diversion. Progress in Physical Geography 19, 449–473.
Drainage rearrangement by river capture, beheading and diversion.Crossref | GoogleScholarGoogle Scholar |

Burridge, C. P., Craw, D., Jack, D. C., King, T. M., and Waters, J. M. (2008). Does fish ecology predict dispersal across a river drainage divide? Evolution 62, 1484–1499.
Does fish ecology predict dispersal across a river drainage divide?Crossref | GoogleScholarGoogle Scholar | 18363866PubMed |

Burrows, D. W. (2004). Translocated fishes in streams of the Wet Tropics region, north Queensland: distribution and potential impact. Cooperative Research Centre for Tropical Rainforest Ecology and Management, Rainforest CRC, Cairns, Qld.

Carini, G., and Hughes, J. M. (2004). Population structure of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia: the role of contemporary and historical processes. Heredity 93, 350–363.
Population structure of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia: the role of contemporary and historical processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVKmsrc%3D&md5=28fabc0f72730e7caf728e7713cb226bCAS | 15329659PubMed |

Carini, G., Hughes, J. M., and Bunn, S. E. (2006). The role of waterholes as ‘refugia’ in sustaining genetic diversity and variation of two freshwater species in dryland river systems (western Queensland, Australia). Freshwater Biology 51, 1434–1446.
The role of waterholes as ‘refugia’ in sustaining genetic diversity and variation of two freshwater species in dryland river systems (western Queensland, Australia).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=391da7bb4e4824710758e3cd00fd0dd4CAS | 11050560PubMed |

Cook, B. D., Bunn, S. E., and Hughes, J. M. (2002). Genetic structure and dispersal of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia. Freshwater Biology 47, 2098–2112.
Genetic structure and dispersal of Macrobrachium australiense (Decapoda: Palaemonidae) in western Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptVKiu78%3D&md5=8690d2d619ab7dab3292fe832c0323afCAS |

Cook, B. D., Pringle, C. M., and Hughes, J. M. (2008). Molecular evidence for sequential colonization and taxon cycling in freshwater decapod shrimps on a Caribbean island. Molecular Ecology 17, 1066–1075.
Molecular evidence for sequential colonization and taxon cycling in freshwater decapod shrimps on a Caribbean island.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVajurc%3D&md5=5dae631079179da262cf6cebf76402bbCAS | 18261048PubMed |

Dimmock, A., Williamson, L., and Mather, B. (2004). The influence of environment on the morphology of Macrobrachium australiense (Decapoda: Palaemonidae). Aquaculture International 12, 435–456.
The influence of environment on the morphology of Macrobrachium australiense (Decapoda: Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

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

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metic distances among DNA haplotypes – application to human mitochondrial-DNA restricted data. Genetics 131, 479–491.
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=250a741994f4e76df8d52eb5da21d9c7CAS | 1644282PubMed |

Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47–50.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=f87d0686d3a2b56a2918430d0ac2db0bCAS |

Finn, D. S., Bonada, N., Murria, 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=6f8e6622cb69660a6980e74859c7145dCAS | 7881515PubMed |

Fraser, D., Cannings, S., Paige, D., Nelson, K., and Harcombe, A. (2004). Risk listing and setting conservation priorities for species in British Columbia: a review of current practices. In ‘Species at Risk 2004 Pathways to Recovery Conference’, 2–6 March 2004. (Ed. T. Hooper.) pp. 1–5. (Species at Risk 2004 Pathways to Recovery Conference Organising Committee: Victoria, BC.)

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=5b6b79963a3469375d36bc0ec5761690CAS | 9335623PubMed |

Gomez-Uchida, D., Knight, T. W., and Ruzzante, D. E. (2009). Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids. Molecular Ecology 18, 4854–4869.
Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids.Crossref | GoogleScholarGoogle Scholar | 19878451PubMed |

Hájek, M., Rolecek, J., Cottenie, K., Kintrova, K., Horsak, M., Poulickova, A., Hajkova, P., Frankova, M., and Dite, D. (2011). Environmental and spatial controls of biotic assemblages in a discrete semi-terrestrial habitat: comparison of organisms with different dispersal abilities sampled in the same plots. Journal of Biogeography 38, 1683–1693.
Environmental and spatial controls of biotic assemblages in a discrete semi-terrestrial habitat: comparison of organisms with different dispersal abilities sampled in the same plots.Crossref | GoogleScholarGoogle Scholar |

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., and Hillyer, M. J. (2006). Mitochondrial DNA and allozymes reveal high dispersal abilities and historical movement across drainage boundaries in two species of freshwater fishes from inland rivers in Queensland, Australia. Journal of Fish Biology 68, 270–291.
Mitochondrial DNA and allozymes reveal high dispersal abilities and historical movement across drainage boundaries in two species of freshwater fishes from inland rivers in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntFaktr8%3D&md5=ce0c5e019f165bd0a542437e2eba6ef5CAS |

Hughes, J. M., Bunn, S. E., Hurwood, D. A., Choy, S., and Pearson, R. G. (1996). Genetic differentiation among populations of Caridina zebra (Decapoda: Atyidae) in tropical rainforest streams, northern Australia. Freshwater Biology 36, 289–296.
Genetic differentiation among populations of Caridina zebra (Decapoda: Atyidae) in tropical rainforest streams, northern Australia.Crossref | GoogleScholarGoogle Scholar |

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 |

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=4346d3f3a32e525bdedbbb1cc899a25aCAS | 9819905PubMed |

Hurwood, D. A., and Hughes, J. M. (2001a). Nested clade analysis of the freshwater shrimp, Caridina zebra (Decapoda: Atyidae), from north-eastern Australia. Molecular Ecology 10, 113–125.
Nested clade analysis of the freshwater shrimp, Caridina zebra (Decapoda: Atyidae), from north-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1ejtLk%3D&md5=3f8e74322a9daf224ccd013ef5aca0dcCAS | 11251792PubMed |

Hurwood, D. A., and Hughes, J. M. (2001b). Historical interdrainage dispersal of eastern rainbowfish from the Atherton Tableland, north-eastern Australia. Journal of Fish Biology 58, 1125–1136.

Hurwood, D. A., Hughes, J. M., Bunn, S. E., 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=384b398a0e3a7bbd88bcf4f7af136b08CAS | 12522427PubMed |

Liu, M. Y., Cai, Y. X., and Tzeng, C. S. (2007). Molecular systematics of the freshwater prawn genus Macrobrachium Bate, 1868 (Crustacea: Decapoda: Palaemonidae) inferred from mtDNA sequences, with emphasis on East Asian species. Zoological Studies 46, 272–289.
| 1:CAS:528:DC%2BD2sXotVCmsb0%3D&md5=a716a47b690cb3c941486d4189295cf2CAS |

Mantel, N. (1967). Detection of disease clustering and a generalized regression approach. Cancer Research 27, 209.
| 1:STN:280:DyaF2s%2FptlSnsA%3D%3D&md5=b445c16f69af1e777fba390ad3c7abbcCAS | 6018555PubMed |

McGlashan, D. J., and Hughes, J. M. (2002). Extensive genetic divergence among populations of the Australian freshwater fish, Pseudomugil signifer (Pseudomugilidae), at different hierarchical scales. Marine and Freshwater Research 53, 897–907.
Extensive genetic divergence among populations of the Australian freshwater fish, Pseudomugil signifer (Pseudomugilidae), at different hierarchical scales.Crossref | GoogleScholarGoogle Scholar |

Meffe, G. K., and Vrijenhoek, R. C. (1988). Conservation genetics in the management of desert fishes. Conservation Biology 2, 157–169.
Conservation genetics in the management of desert fishes.Crossref | GoogleScholarGoogle Scholar |

Murphy, N. P., and Austin, C. M. (2004). Multiple origins of the endemic Australian Macrobrachium (Decapoda: Palaemonidae) based on 16S rRNA mitochondrial sequences. Australian Journal of Zoology 52, 549–559.
Multiple origins of the endemic Australian Macrobrachium (Decapoda: Palaemonidae) based on 16S rRNA mitochondrial sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFOhu70%3D&md5=dce46fc499383804d8a8b0643e56e487CAS |

Murphy, N. P., and Austin, C. M. (2005). Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development. Zoologica Scripta 34, 187–197.
Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development.Crossref | GoogleScholarGoogle Scholar |

Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=a47a59923d054de0e36c058dfec4811fCAS | 10706275PubMed |

Ollier, C. D. (1978). Tectonics and geomorphology of the eastern highlands. In ‘Landform Evolution in Australia’. (Eds. J. L. Davies and M. A. J. Williams.) pp. 5–47. (ANU Press: Canberra.)

Ollier, C. D. (1979). Evolutionary geomorphology of Australia and Papua-New-Guinea. Transactions of the Institute of British Geographers 4, 516–539.
Evolutionary geomorphology of Australia and Papua-New-Guinea.Crossref | GoogleScholarGoogle Scholar |

Page, R., and Holmes, E. (1998). ‘Molecular Evolution: a Phylogeographic Approach.’ (Blackwell Press: Oxford, UK.)

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 |

Queensland Museum (2004). ‘Wildlife of Tropical North Queensland.’ (Queensland Museum: Brisbane.)

Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.
| 1:STN:280:DyaK2s3kslOntQ%3D%3D&md5=540865e20cbb801032bf861bd3a6572eCAS | 9093870PubMed |

Safont, E., Vegas-Vilarrubia, T., and Rull, V. (2012). Use of environmental impact assessment (EIA) tools to set priorities and optimize strategies in biodiversity conservation. Biological Conservation 149, 113–121.
Use of environmental impact assessment (EIA) tools to set priorities and optimize strategies in biodiversity conservation.Crossref | GoogleScholarGoogle Scholar |

Sharma, S., and Hughes, J. M. (2009). Genetic structure and phylogeography of freshwater shrimps (Macrobrachium australiense and Macrobrachium tolmerum): the role of contemporary and historical events. Marine and Freshwater Research 60, 541–553.
Genetic structure and phylogeography of freshwater shrimps (Macrobrachium australiense and Macrobrachium tolmerum): the role of contemporary and historical events.Crossref | GoogleScholarGoogle Scholar |

Short, J. W. (2004). A revision of Australian river prawns, Macrobrachium (Crustacea: Decapoda: Palaemonidae). Hydrobiologia 525, 1–100.
A revision of Australian river prawns, Macrobrachium (Crustacea: Decapoda: Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Slatkin, M. (1987). Gene flow and the geographic structure of natural-populations. Science 236, 787–792.
Gene flow and the geographic structure of natural-populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3gs1Wruw%3D%3D&md5=6da006a5e960b4816be86c9450ed6dc7CAS | 3576198PubMed |

Slatkin, M. (1993). Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264–279.
Isolation by distance in equilibrium and nonequilibrium populations.Crossref | GoogleScholarGoogle Scholar |

Smock, L. A. (1994). Movements of invertebrates between stream channels and forested floodplains. Journal of the North American Benthological Society 13, 524–531.
Movements of invertebrates between stream channels and forested floodplains.Crossref | GoogleScholarGoogle Scholar |

Smouse, P. E., Long, J. C., and Sokal, R. R. (1986). Multiple-regression and correlation extensions of themantel test of matrix correspondence. Systematic Zoology 35, 627–632.
Multiple-regression and correlation extensions of themantel test of matrix correspondence.Crossref | GoogleScholarGoogle Scholar |

Stanwell Corporation Limited (2004). Koombooloomba Hydro. Available at http://www.stanwell.com/frame.asp?ContentURL=/sites/koombooloomba.asp [Verified 28 May 2008].

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=8b607e6188546f8647101405a1596d5bCAS | 2513255PubMed |

Thermo Fisher Scientific Inc. (2014). Faster cycle sequencing applications using the Applied Biosystems 9800 Fast Thermal Cycler. Available at http://tools.lifetechnologies.com/content/sfs/manuals/cms_041944.pdf [Verified 7 March 2014].

Walck, J. L., Baskin, J. M., and Baskin, C. C. (2001). Why is Solidago shortii narrowly endemic and S-altissima geographically widespread? A comprehensive comparative study of biological traits. Journal of Biogeography 28, 1221–1237.
Why is Solidago shortii narrowly endemic and S-altissima geographically widespread? A comprehensive comparative study of biological traits.Crossref | GoogleScholarGoogle Scholar |

Whitehead, P. W., Stephenson, P. J., McDougall, I., Hopkins, M. S., Grahams, A. W., Collerson, K. D., and Johnson, D. P. (2007). Temporal development of the Atherton Basalt Province, North Queensland. Australian Journal of Earth Sciences 54, 691–709.
Temporal development of the Atherton Basalt Province, North Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFyit7g%3D&md5=0a7b8f76086e82855a3760914ac7b3b5CAS |

Wulff, A. S., Hollingsworth, P. M., Ahrends, A., Jaffre, T., Veillon, J. M., L'Huillier, L., and Fogliani, B. (2013). Conservation priorities in a biodiversity hotspot: analysis of narrow endemic plant species in New Caledonia. PLoS ONE 8, .
Conservation priorities in a biodiversity hotspot: analysis of narrow endemic plant species in New Caledonia.Crossref | GoogleScholarGoogle Scholar | 24058470PubMed |