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Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (Gambusia holbrooki) in the greater Melbourne area, Australia

Abstract

Eastern mosquitofish (Gambusia holbrooki) were introduced into Australia in 1925 and released to control mosquitoes. Gambusia holbrooki rapidly became invasive in recipient environments and now threaten native fauna. In this study, we used five polymorphic microsatellite loci and sequence from two mitochondrial genes, cytochrome b and cytochrome oxidase I, to evaluate genetic variation, colonisation and movement patterns of introduced G. holbrooki in the greater Melbourne area, and to assist in identifying the feasibility of local eradication. Microsatellite variation was consistently low within populations and there was evidence of bottleneck events for several populations. Populations displayed significant structuring associated with river basins rather than geographic distance, suggesting that habitat connectivity is important for dispersal. However, a few populations within river basins were more closely related to populations in other river basins than within their own basin, most likely reflecting a role of human-assisted dispersal in population establishment. Mitochondrial sequencing revealed only a single haplotype and suggested all populations were founded by individuals from a common source. These genetic data help delineate boundaries for local management strategies.

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References

  • Ahern RG, Hawthorne DJ, Raupp MJ (2009) Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States. Biol Invasions 11:959–971

    Article  Google Scholar 

  • Alemadi S, Jenkins D (2008) Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae). Biol Invasions 10:59–66

    Article  Google Scholar 

  • Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences in small population size in plants: implications for conservation. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 1–30

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.03, Logiciel Sous Windows™ Pour la Génétique Des Populations., Laboratoire Génome et Populations. Université de Montpellier II, Montpellier

    Google Scholar 

  • Bøhn T, Amundsen PA, Sparrow A (2008) Competitive exclusion after invasion? Biol Invasions 10:359–368

    Article  Google Scholar 

  • Brown JE, Stepien CA (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Mol Ecol 18:64–79

    CAS  PubMed  Google Scholar 

  • Bryan MB, Zalinski D, Filcek KB, Libants S, Li W, Scribner KT (2005) Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes. Mol Ecol 14:3757–3773

    CAS  Article  PubMed  Google Scholar 

  • Chapman P, Warburton K (2006) Postflood movements and population connectivity in gambusia (Gambusia holbrooki). Ecol Fresh Fish 15:357–365

    Article  Google Scholar 

  • Congdon BC (1992) The maintenance of genetic diversity in subdivided populations of the mosquitofish Gambusia holbrooki. PhD thesis, Griffith University, Brisbane, Queensland, Australia

  • Congdon BC (1995) Unidirectional gene flow and maintenance of genetic diversity in mosquitofish Gambusia holbrooki (Teleostei: Poeciliidae). Copeia: 162–172

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Crowl TA, Townsend CR, McIntosh AR (1992) The impact of introduced brown and rainbow trout on native fish: the case of Australasia. Rev Fish Biol Fish 2:217–241

    Article  Google Scholar 

  • DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473

    CAS  Article  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    CAS  Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    CAS  Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Fausch KD (2007) Introduction, establishment and effects of non-native salmonids: considering the risk of rainbow trout invasion in the United Kingdom. J Fish Biol 71(Supplement D):1–32. doi:10.1111/j.1095-8649.2007.01682.x

    Article  Google Scholar 

  • Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385. doi:10.1038/sj.hdy.6800634

    CAS  Article  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-Statistics. J Hered 86:485–486

    Google Scholar 

  • Grapputo A, Bisazza A, Pilastro A (2006) Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbrooki). Ital J Zool 73:67–73

    CAS  Article  Google Scholar 

  • Greiner R, Gregg D (2008) Tilapia in north Queensland waterways: risks and potential economic impacts. Report prepared for the Australian Centre for Tropical Freshwater Research. River Consulting, Townsville

  • Gunnell K (2008) Geographic patterns of introgressive hybridization between native Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and introduced rainbow trout (O. mykiss) in the South Fork of the Snake River watershed, Idaho. Conserv Genetics 9:49–64

    CAS  Article  Google Scholar 

  • Hanfling B (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71:115–135

    Article  Google Scholar 

  • Hayes KR, Cannon R, Neil K, Inglis G (2005) Sensitivity and cost considerations for the detection and eradication of marine pests in ports. Mar Poll Bull 50:823–834

    CAS  Google Scholar 

  • Haynes GD, Gilligan DM, Grewe P, Nicholas FW (2009) Population genetics and management units of invasive common carp Cyprinus carpio in the Murray-Darling Basin, Australia. J Fish Biol 75:295–320

    CAS  Article  PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B: Biol Sci 270:313–321

    CAS  Article  Google Scholar 

  • Hernandez-Martich JD, Smith MH (1990) Patterns of genetic-variation in Eastern mosquitofish (Gambusia holbrooki Girard) from the Piedmont and Coastal Plain of three drainages. Copeia: 619–630

  • Hernandez-Martich JD, Smith MH (1997) Downstream gene flow and genetic structure of Gambusia holbrooki (eastern mosquitofish) populations. Heredity 79:295–301

    Article  Google Scholar 

  • Hood GM (2006) PopTools version 2.7.5 Available on the internet. URL http://www.cse.csiro.au/poptools

  • Keane JP, Neira FJ (2004) First record of mosquitofish, Gambusia holbrooki, in Tasmania, Australia: stock structure and reproductive biology. New Zeal J Mar Fresh 38:857

    Article  Google Scholar 

  • Kimura M (1980) A simple method of estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  Article  PubMed  Google Scholar 

  • Koehn JD, MacKenzie RF (2004) Priority management actions for alien freshwater fish species in Australia. New Zeal J Mar Fresh 38:457

    Article  Google Scholar 

  • Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S (2008) Fish invasions in the World’s river systems: when natural processes are blurred by human activities. PLoS Biol 6:404–410. doi:10.1371/journal.pbio.0060028

    CAS  Google Scholar 

  • Lindholm AK, Breden F, Alexander HJ, Chan WK, Thakurta SG, Brooks R (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682

    CAS  Article  PubMed  Google Scholar 

  • Lintermans M, Rutzou T (1990) Removal of feral fish from artifical ponds in the Australian National Botanic Gardens. ACT Parks and Conservation Service. Wildlife Unit, Canberra

    Google Scholar 

  • Lloyd LN, Tomasov JF (1985) Taxanomic status of the mosquitofish, Gambusia affinis (Poeciliidae), in Australia. Aust J Mar Freshw Res 36:447–451

    Article  Google Scholar 

  • Lydeard C, Wooten MC, Meyer A (1995) Cytochrome B sequence variation and a molecular phylogeny of the live-bearing fish genus Gambusia (Cyprinodontiformes, Poeciliidae). Can J Zool 73:213–227

    CAS  Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Milner R (2006) Gambusia holbrooki: a management guide and workbook. Natural Heritage Trust, Launceston

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pen LJ, Potter IC (1992) Seasonal and size-related changes in the diet of perch. Perca fluviatilis L., in the shallows of an Australian river, and their implications for the conservation of indigenous teleosts. Aq Conserv Mar Fresh Ecos 2:243–253

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Pyke GH (2008) Plague minnow or mosquito fish? a review of the biology and impacts of introduced Gambusia species. Ann Rev Ecol Evol Syst 39:171–191

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reaser JK, Meyerson LA, Cronk Q, De Poorter M, Eldrege LG, Green E, Kairo M, Latasi P, Mack RN, Mauremootoo J, O’Dowd D, Orapa W, Sastroutomo S, Saunders A, Shine C, Thrainsson S, Vaiutu L (2007) Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environ Conserv 34:98–111

    Article  Google Scholar 

  • Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Rosen DE, Bailey RM (1963) The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography & systematics. Bull Am Mus Nat Hist. 126:1–176

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Rowe DK, Moore A, Giorgetti A, Maclean C, Grace P, Wadhwa S, Cooke J (2008) Review of the impacts of gambusia, redfin perch, tench, roach, yellowfin goby and streaked goby in Australia. Prepared for the Australian Government Department of the Environment, Water, Heritage and the Arts, Canberra

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, LeRoy Poff N, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    CAS  Article  PubMed  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hasting SA, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed  Google Scholar 

  • Smith MH, Scribner KT, Hernandez JD, Wooten MC (1989) Demographic, spatial and temporal genetic variation in Gambusia. In: Meffe GK, Snelson FF (eds) Ecology and evolution of livebearing fishes (Poeciliidae). Prentice-Hall Inc., Englewood Cliffs, pp 235–362

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W. H. Freeman, San Francisco, p 776

    Google Scholar 

  • Spencer CC, Chlan CA, Neigel JE, Scribner KT, Wooten MC, Leberg PL (1999) Polymorphic microsatellite markers in the western mosquitofish, Gambusia affinis. Mol Ecol 8:157–168

    CAS  PubMed  Google Scholar 

  • Starling F, Lazzaro X, Cavalcanti C, Moreira R (2002) Contribution of omnivorous tilapia to eutrophication of a shallow tropical reservoir: evidence from a fish kill. Fresh Biol 47:2443–2452

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    CAS  Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    CAS  Article  PubMed  Google Scholar 

  • Valade R, Kenis M, Hernandez-Lopez A, Augustin S, Mari Mena N, Magnoux E, Rougrie R, Lakatos F, Roques A, Lopez-Vaamonde C (2009) Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Mol Ecol 18:3458–3470

    CAS  Article  PubMed  Google Scholar 

  • Valero A, Macías Garcia C, Magurran AE (2008) Heterospecific harassment of native endangered fishes by invasive guppies in Mexico. Biol Lett 4:149–152

    Article  PubMed  Google Scholar 

  • Vidal O, García-Berthou E, Tedesco PA, García-Marín JL (2009) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions. doi: 10.1007/s10530-009-9505-5

  • Walsh PS, Metzger DA, Highuchi R (1991) Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Phil Trans R Soc B: Biol Sci 360:1847–1857

    CAS  Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Welcomme RL (1988) International introductions of inland aquatic species. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Whittington RJ, Chong R (2007) Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 81:92–116

    CAS  Article  PubMed  Google Scholar 

  • Wilson F (1960) A review of the biological control of insects and weeds in Australia and Australian New Guinea. Commonwealth Agricultural Bureaux, Bucks 102

    Google Scholar 

  • Zane L, Nelson WS, Jones AG, Avise JC (1999) Microsatellite assessment of multiple paternity in natural populations of a live-bearing fish, Gambusia holbrooki. J Evol Biol 12:61–69

    Article  Google Scholar 

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Acknowledgments

We thank Steve Marshall, Trish Grant, and John McGuckin for providing some sample collections. We also thank Kathryn Guthridge, Paul Mitrovski and Andrew Weeks for guidance on project methods, Melissa Carew for comments on the draft manuscript and David Sharley for assistance generating Fig. 1. STRUCTURE analysis was carried out using the resources of the Computational Biology Service Unit from Cornell University which is partially funded by Microsoft Corporation. Two anonymous reviewers contributed considerably to the improvement of the manuscript. This work was funded by the Melbourne Water Corporation.

Appendix

See Tables 4, 5.

Table 4 Allele frequencies at five polymorphic microsatellite loci in Gambusia holbrooki populations. Populations (L as described in Table 1) are separated into river basins
Table 5 Genetic differentiation estimated using Wright’s F ST statistic (lower diagonal) and the geographic distance (km) (upper diagonal) between population pairs of Gambusia holbrooki. Populations (L as described in Table 1) are separated into river basins

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Ayres, R.M., Pettigrove, V.J. & Hoffmann, A.A. Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (Gambusia holbrooki) in the greater Melbourne area, Australia. Biol Invasions 12, 3727–3744 (2010). https://doi.org/10.1007/s10530-010-9766-z

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Keywords

  • Gambusia holbrooki
  • Eastern mosquitofish
  • Invasive
  • Microsatellites
  • Mitochondrial DNA
  • Australia