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RESEARCH ARTICLE

Genetic structure and diversity of introduced eastern mosquitofish (Gambusia holbrooki) in south-eastern Australia

Renae M. Ayres A B D , Vincent J. Pettigrove C and Ary A. Hoffmann A C
+ Author Affiliations
- Author Affiliations

A Department of Zoology, University of Melbourne, Bio21 Institute, 30 Flemington Road, Parkville, Vic. 3010, Australia.

B Present address: Department of Sustainability and Environment, Arthur Rylah Institute for Environmental Research, 123 Brown Street, Heidelberg, Vic. 3084, Australia.

C Victorian Centre for Aquatic Pollution Identification and Management, University of Melbourne, Bio21 Institute, 30 Flemington Road, Parkville, Vic. 3010, Australia.

D Corresponding author. Email: renae.ayres@dse.vic.gov.au

Marine and Freshwater Research 63(12) 1206-1214 https://doi.org/10.1071/MF11279
Submitted: 16 December 2011  Accepted: 24 September 2012   Published: 12 December 2012

Abstract

The closely related eastern mosquitofish (Gambusia holbrooki) and western mosquitofish (Gambusia affinis) have been introduced into many countries and collectively represent the most widely distributed freshwater fish in the world. We investigated genetic patterns associated with the spread of G. holbrooki in its introduced range in south-eastern Australia, by sampling 60 G. holbrooki populations (n = 1771) from major regions where G. holbrooki was initially introduced into Australia, and characterising the genetic diversity and population structure of G. holbrooki, using five polymorphic nuclear microsatellite loci and sequences from two mitochondrial genetic markers. Results were compared with published data on American and European Gambusia samples and historical records. Low microsatellite diversity and strong population genetic structuring were found within G. holbrooki in south-eastern Australia. Observed heterozygosity and allelic richness declined regionally in the order Sydney, Brisbane, Canberra, Melbourne and Adelaide. Microsatellite variation in Australia was reduced compared with native populations. Two mitochondrial DNA haplotypes of G. holbrooki were found; one was common, whereas the other was detected in one Sydney population and one Melbourne population. Cytochrome b sequence diversity was reduced compared with native and European ranges, and sequences were identical to two haplotypes previously identified. Microsatellite diversity of G. holbrooki in south-eastern Australia validates historical records of its spread, beginning north and moving south. Mitochondrial sequencing confirms that G. holbrooki is present in Australia, but the origins of Australian G. holbrooki populations remain unclear.

Additional keywords : colonisation history, genetic diversity, microsatellites, mitochondrial DNA.


References

Alemadi, S., and Jenkins, D. (2008). Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae). Biological Invasions 10, 59–66.
Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae).Crossref | GoogleScholarGoogle Scholar |

Arthington, A. H., Kailola, P. J., Woodland, D. J., and Zalucki, J. M. (1999). Baseline environmental data relevant to an evaluation of quarantine risk potentially associated with the importation to Australia of ornamental finfish. Report to the Australian Quarantine and Inspection Service, Department of Agriculture, Fisheries and Forestry. Griffith University, University of New England, Canberra.

Ayres, R. M., Pettigrove, V. J., and Hoffmann, A. A. (2010). Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (Gambusia holbrooki) in the greater Melbourne area, Australia. Biological Invasions 12, 3727–3744.
Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (Gambusia holbrooki) in the greater Melbourne area, Australia.Crossref | GoogleScholarGoogle Scholar |

Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., and Bonhomme, F. (2004). ‘GENETIX 4.03, Logiciel Sous WindowsTM Pour la Génétique Des Populations.’ (Université de Montpellier II: Montpellier, France.)

Casal, C. M. V. (2006). Global documentation of fish introductions: the growing crisis and recommendations for action. Biological Invasions 8, 3–11.
Global documentation of fish introductions: the growing crisis and recommendations for action.Crossref | GoogleScholarGoogle Scholar |

Congdon, B. C. (1992). The maintenance of genetic diversity in subdivided populations of the mosquitofish Gambusia holbrooki. Ph.D. Thesis, Griffith University, Brisbane.

Congdon, B. C. (1994). Characteristics of dispersal in the eastern mosquitofish Gambusia holbrooki. Journal of Fish Biology 45, 943–952.
Characteristics of dispersal in the eastern mosquitofish Gambusia holbrooki.Crossref | GoogleScholarGoogle Scholar |

Cornuet, J. M., and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.
| 1:STN:280:DyaK2s7jt1Kgsw%3D%3D&md5=d2eeb50d8bcf18c45775408ccae9dce0CAS |

Cote, J., Fogarty, S., Weinersmith, K., Brodin, T., and Sih, A. (2010). Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proceedings. Biological Sciences 277, 1571–1579.
Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis).Crossref | GoogleScholarGoogle Scholar |

Courtenay, W. R. J., and Meffe, G. K. (1989). Small fishes in strange places: a review of introduced poeciliids. In ‘Ecology and Evolution of Live Bearing Fishes (Poeciliidae)’. (Eds G. K. Meffe and F. F. Snelson.) pp. 319–332. (Prentice Hall: NJ.)

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software structure: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=97d778092ae53c6cfb96559182803610CAS |

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=9c0640beefdd6f7f3c14397c8117bf33CAS |

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.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=257574cbf5e00e342cf2948ca3eed01bCAS |

García-Berthou, E., Alcaraz, C., Pou-Rovira, Q., Zamora, L., Coenders, G., and Feo, C. (2005). Introduction pathways and establishment rates of invasive aquatic species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 62, 453–463.
Introduction pathways and establishment rates of invasive aquatic species in Europe.Crossref | GoogleScholarGoogle Scholar |

Gherardi, F. (2007). Biological invasions in inland waters: an overview. In ‘Biological Invaders in Inland Waters: Profiles, Distribution and Threats’. (Ed. F. Gherardi.) pp. 3–25. (Springer: The Netherlands.)

Goudet, J. (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.

Gozlan, R. E. (2008). Introduction of non-native freshwater fish: is it all bad? Fish and Fisheries 9, 106–115.
Introduction of non-native freshwater fish: is it all bad?Crossref | GoogleScholarGoogle Scholar |

Grapputo, A., Bisazza, A., and Pilastro, A. (2006). Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbrooki). The Italian Journal of Zoology 73, 67–73.
Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbrooki).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVOrsLg%3D&md5=b4f343fa6bb9620ac520efe03e6785a2CAS |

Hohausová, E., Lavoy, R. J., and Allen, M. S. (2010). Fish dispersal in a seasonal wetland: influence of anthropogenic structures. Marine and Freshwater Research 61, 682–694.
Fish dispersal in a seasonal wetland: influence of anthropogenic structures.Crossref | GoogleScholarGoogle Scholar |

Hood, G. M. (2006). ‘PopTools, version 2.7.5.’ Available at http://www.cse.csiro.au/poptools (accessed 23 October 2007).

Hubbs, C. L. (1955). Hybridization between fish species in nature. Systematic Zoology 4, 1–20.
Hybridization between fish species in nature.Crossref | GoogleScholarGoogle Scholar |

Jeschke, J. M., and Strayer, D. L. (2005). From the cover: Invasion success of vertebrates in Europe and North America. Proceedings of the National Academy of Sciences, USA 102, 7198–7202.
From the cover: Invasion success of vertebrates in Europe and North America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks12ns78%3D&md5=4e180587fdaefc5b1d81fbda46349a33CAS |

Keane, J. P., and Neira, F. J. (2004). First record of mosquitofish, Gambusia holbrooki, in Tasmania, Australia: stock structure and reproductive biology. New Zealand Journal of Marine and Freshwater Research 38, 857–867.
First record of mosquitofish, Gambusia holbrooki, in Tasmania, Australia: stock structure and reproductive biology.Crossref | GoogleScholarGoogle Scholar |

Kimura, M. (1980). A simple method of estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method of estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=70887689120a12a4a5216dc17017bfc4CAS |

Koehn, J. D., and MacKenzie, R. F. (2004). Priority management actions for alien freshwater fish species in Australia. New Zealand Journal of Marine and Freshwater Research 38, 457–472.
Priority management actions for alien freshwater fish species in Australia.Crossref | GoogleScholarGoogle Scholar |

Krumholz, L. A. (1948). Reproduction in the western mosquitofish, Gambusia affinis affinis (Baird & Girard), and its use in mosquito control. Ecological Monographs 18, 1–43.
Reproduction in the western mosquitofish, Gambusia affinis affinis (Baird & Girard), and its use in mosquito control.Crossref | GoogleScholarGoogle Scholar |

Lloyd, L. N., and Tomasov, J. F. (1985). Taxanomic status of the mosquitofish, Gambusia affinis (Poeciliidae), in Australia. Australian Journal of Marine and Freshwater Research 36, 447–451.
Taxanomic status of the mosquitofish, Gambusia affinis (Poeciliidae), in Australia.Crossref | GoogleScholarGoogle Scholar |

Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.
| 1:STN:280:DyaF2s%2FptlSnsA%3D%3D&md5=73511f8ed0a2bf15b566fddb8d4eb0ecCAS |

Milton, D. A., and Arthington, A. H. (1983). Reproductive biology of Gambusia affinis holbrooki Baird and Girard, Xiphophorus helleri (Gunther) and X. maculatus (Heckel) (Pisces; Poeciliidae) in Queensland, Australia. Journal of Fish Biology 23, 23–41.
Reproductive biology of Gambusia affinis holbrooki Baird and Girard, Xiphophorus helleri (Gunther) and X. maculatus (Heckel) (Pisces; Poeciliidae) in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Okada, M., Lyle, M., and Jasieniuk, M. (2009). Inferring the introduction history of the invasive apomictic grass Cortaderia jubata using microsatellite markers. Diversity & Distributions 15, 148–157.
Inferring the introduction history of the invasive apomictic grass Cortaderia jubata using microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Parenti, L. R., and Rauchenberger, M. (1989). Systematics overview of the Poeciliines. In ‘Ecology and Evolution of Livebearing Fishes (Poeciliidae)’. (Eds G. K. Meffe and F. F. Snelson Jr.) pp. 3–12. (Prentice Hall: NJ.)

Peacock, M. M., Beard, K. H., O’Neill, E. M., Kirchoff, V. S., and Peters, M. B. (2009). Strong founder effects and low genetic diversity in introduced populations of Coqui frogs. Molecular Ecology 18, 3603–3615.
Strong founder effects and low genetic diversity in introduced populations of Coqui frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WhtrnO&md5=0a5638dbc4856a48b5f4945f8cde4d92CAS |

Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Prentis, P. J., Sigg, D. P., Raghu, S., Dhileepan, K., Pavasovic, A., and Lowe, A. J. (2009). Understanding invasion history: genetic structure and diversity of two globally invasive plants and implications for their management. Diversity & Distributions 15, 822–830.
Understanding invasion history: genetic structure and diversity of two globally invasive plants and implications for their management.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=2e7d2738a7939d38ab608f04cb82fdfaCAS |

Purcell, K., Ling, N., and Stockwell, C. (2012). Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biological Invasions 14, 2057–2065.

Pyke, G. H. (2005). A review of the biology of Gambusia affinis and Gambusia holbrooki. Reviews in Fish Biology and Fisheries 15, 339–365.
A review of the biology of Gambusia affinis and Gambusia holbrooki.Crossref | GoogleScholarGoogle Scholar |

Pyke, G. H. (2008). Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annual Review of Ecology Evolution and Systematics 39, 171–191.
Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species.Crossref | GoogleScholarGoogle Scholar |

Rauchenberger, M. (1989). Systematics and biogeography of the genus Gambusia (Cyprinodontoformes: Poecilidae). American Museum Novitates 2951, 1–74.

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.

Rehage, J. S., and Sih, A. (2004). Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biological Invasions 6, 379–391.
Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species.Crossref | GoogleScholarGoogle Scholar |

Rosen, D. E., and Bailey, R. M. (1963). The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography & systematics. Bulletin of the American Museum of Natural History 126, 1–176.

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=c43aa8096e4c0abac28f6db5e4442efcCAS |

Ruesink, J. L. (2005). Global analysis of factors affecting the outcome of freshwater fish introductions. Conservation Biology 19, 1883–1893.
Global analysis of factors affecting the outcome of freshwater fish introductions.Crossref | GoogleScholarGoogle Scholar |

Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O’Neil, P., Parker, I. M., Thompson, J. N., and Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.
The population biology of invasive species.Crossref | GoogleScholarGoogle Scholar |

Simberloff, D. (2009). The role of propagule pressure in biological invasions. Annual Review of Ecology Evolution and Systematics 40, 81–102.
The role of propagule pressure in biological invasions.Crossref | GoogleScholarGoogle Scholar |

Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462.
| 1:STN:280:DyaK2M3itVKrtw%3D%3D&md5=df47c5f3877636cdd86448286410d600CAS |

Sokal, R. R., and Rohlf, F. J. (1995). ‘Biometry: the Principles and Practice of Statistics in Biological Research.’ (W.H. Freeman: San Francisco, CA.)

Spencer, C. C., Chlan, C. A., Neigel, J. E., Scribner, K. T., Wooten, M. C., and Leberg, P. L. (1999). Polymorphic microsatellite markers in the western mosquitofish, Gambusia affinis. Molecular Ecology 8, 157–168.
| 1:CAS:528:DyaK1MXjtVOgurk%3D&md5=6bc8dfcfb5fcce87a9c4d22db36adbc6CAS |

Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=ad965f33eede4cdde4fa49ff1fa322dbCAS |

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=21ef800f00164adb8760c4d4d5adffe1CAS |

Vidal, O., García-Berthou, E., Tedesco, P. A., and García-Marín, J. L. (2010). Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biological Invasions 12, 841–851.
Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe.Crossref | GoogleScholarGoogle Scholar |

Vidal, O., Sanz, N., Araguas, R. M., Fernández-Cebrian, R., Diez-del-Molino, D., and García-Marín, J. L. (2011). SNP diversity in introduced populations of the invasive Gambusia holbrooki. Ecology Freshwater Fish , .
SNP diversity in introduced populations of the invasive Gambusia holbrooki.Crossref | GoogleScholarGoogle Scholar |

Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R., and Hebert, P. D. N. (2005). DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1847–1857.
DNA barcoding Australia’s fish species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSjsrjK&md5=63876412781251c28f9d70363611436eCAS |

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Welcomme, R. L. (1988). ‘International Introductions of Inland Aquatic Species.’ (Food and Agriculture Organization of the United Nations: Rome.)

Wilson, F. (1960). ‘A review of the Biological Control of Insects and Weeds in Australia and Australian New Guinea.’ (Commonwealth Agricultural Bureaux: Bucks, UK.)

Wooten, M. C., Scribner, K. T., and Smith, M. H. (1988). Genetic variability and systematics of Gambusia in the southeastern United States. Copeia 1988, 283–289.
Genetic variability and systematics of Gambusia in the southeastern United States.Crossref | GoogleScholarGoogle Scholar |

Zane, L., Nelson, W. S., Jones, A. G., and Avise, J. C. (1999). Microsatellite assessment of multiple paternity in natural populations of a live-bearing fish, Gambusia holbrooki. Journal of Evolutionary Biology 12, 61–69.
Microsatellite assessment of multiple paternity in natural populations of a live-bearing fish, Gambusia holbrooki.Crossref | GoogleScholarGoogle Scholar |