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Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand

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Abstract

Understanding the introduction history and the impact of founder events on invasive species is crucial to understanding the evolutionary mechanisms driving successful invasions. Recently, there has been increased discussion of the “paradox” of invasions, the high success of introduced populations that presumably have limited genetic diversity associated with founder events. The western mosquitofish Gambusia affinis is an ideal species for evaluating this paradox, because it has been widely introduced from its native range in central Texas, USA. This species was introduced to the North Island of New Zealand, circa 1930, and has since invaded aquatic habitats across the North Island. We conducted a microsatellite assay of populations from both the native and introduced range to verify the documented history of invasion and to assess the impact of serial introduction events on the genetic diversity of recently established New Zealand populations. The molecular data were consistent with the documented introduction history. In addition, we found sharp reductions in the allelic richness and the heterozygosity of the introduced populations relative to the original native populations, indicating the presence of founder effects. We also observed the development of strong genetic structure within the introduced range, which is absent within the native range. Finally, we applied approximate Bayesian computation to the introduction scenario to estimate the long-term effective population sizes for the sampled populations.

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References

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

    Article  Google Scholar 

  • Alò D, Turner TF (2005) Effects of habitat fragmentation on effective population size in the endangered rio grande silvery minnow. Conserv Bio 19(4):1138–1148

    Google Scholar 

  • Beaumont MA, Cornuet J-M, Marin J-M, Robert CP (2009) Adaptive approximate Bayesian computation. Biometrika 96:983–990

    Article  Google Scholar 

  • Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19:2609–2625

    Article  PubMed  CAS  Google Scholar 

  • Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002–1015

    Article  PubMed  CAS  Google Scholar 

  • Cavalli-Sforza LL (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Article  Google Scholar 

  • Chesser RK, Smith MW, Smith MH (1984) Biochemical genetics of mosquitofish III. Incidence and significance of multiple insemination. Genetica 64:77–81

    Article  Google Scholar 

  • Clegg SM, Degnan SM, Kikkawa J, Moritz C, Estoup A, Owens IPF (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Natl Acad Sci 99:8127–8132

    Article  PubMed  CAS  Google Scholar 

  • Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    PubMed  CAS  Google Scholar 

  • Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539

    Article  Google Scholar 

  • Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719

    Article  PubMed  CAS  Google Scholar 

  • Csilléry K, Blum MGB, Gaggiotti OE, Francois O (2010) Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol 25:410–418

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19(19):4113–4130

    Google Scholar 

  • Felsenstein J (2004) PHYLIP. Department of Genome Sciences, University of Washington, Seattle

    Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: Island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R (2005) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755

    Article  PubMed  CAS  Google Scholar 

  • Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Holle BV (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17

    Article  PubMed  CAS  Google Scholar 

  • Gaither MR, Bowen BW, Toonen RJ, Planes S, Messmer V, Earle J, Ross Robertson D (2010) Genetic consequences of introducing allopatric lineages of Bluestriped Snapper (Lutjanus kasmira) to Hawaii. Mol Ecol 19:1107–1121

    Article  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A (2009) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99

    Article  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater Prairie-chickens. Mol Ecol 13(9):2617–2630

    Google Scholar 

  • Juliano R, Guerrero Iii R, Ronquillo I (1989) The introduction of exotic aquatic species in the Philippines. Exotic Aquatic Organisms in Asia. Asian Fisheries Society, pp 83–87

  • Kalinowski ST (2002) Evolutionary and statistical properties of three genetic distances. Mol Ecol 11:1263–1273

    Article  PubMed  Google Scholar 

  • Keller SR, Taylor DR (2010) Genomic admixture increases fitness during a biological invasion. J Evol Biol 23:1720–1731

    Article  PubMed  CAS  Google Scholar 

  • King S (1997) Sex ratio and developmental stability in Gambusia affinis affinis. University of Waikato, New Zealand

    Google Scholar 

  • Kolbe JJ, Glor RE, Rodriguez Schettino L, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  PubMed  CAS  Google Scholar 

  • Krumholz LA (1948) Reproduction in the Western Mosquitofish, Gambusia affinis affinis (Baird & Girard), and Its Use in Mosquito Control. Ecol Monogr 18:1

    Article  Google Scholar 

  • Lambert DM, King T, Shepherd LD, Livingston A, Anderson S, Craig JL (2005) Serial population bottlenecks and genetic variation: translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufusater). Conserv Genet 6:1–14

    Article  Google Scholar 

  • Latch E, Dharmarajan G, Glaubitz J, Rhodes O (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302

    Article  Google Scholar 

  • Leberg PL (1990) Influence of genetic variability on population growth: implications for conservation. J Fish Biol 37:193–195

    Article  Google Scholar 

  • Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477–494

    Article  Google Scholar 

  • Leberg PL (1993) Strategies for population reintroduction: effects of genetic variability on population growth and size. Conserv Biol 7:194–199

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    PubMed  CAS  Google Scholar 

  • McDowall RM (1984) Exotic fishes: the New Zealand experience. Distribution, Biology, and Management of Exotic Fishes. Johns Hopkins University Press, Baltimore, pp 200–214

  • McDowall RM (1990) New Zealand freshwater fishes: a natural history and guide. MAF Pub. Group

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

    Article  Google Scholar 

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    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 

  • Purcell KM, Lance SL, Jones KL, Stockwell CA (2011) Ten novel microsatellite markers for the western mosquitofish Gambusia affinis. Conserv Genet Resour 3:361–363

    Article  Google Scholar 

  • Pyke G (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15:339–365

    Article  Google Scholar 

  • Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu 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 

  • Reusch TBH, Bolte SR, Sparwel M, Moss AG, Javidpour J (2010) Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world’s most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Mol Ecol 19:2690–2699

    Article  PubMed  CAS  Google Scholar 

  • Robbins LW, Hartman GD, Smith MH (1987) Dispersal, reproductive strategies, and the maintenance of genetic variability in mosquitofish (Gambusia affinis). Copeia 1987:156–164

    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 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363

    Article  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, 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 

  • Scribner KT, Wooten MC, Smith MH, Kennedy PK, Rhodes OE (1992) Variation in life history and genetic traits of Hawaiian mosquitofish populations. J Evol Biol 5:267–288

    Article  Google Scholar 

  • Seale A (1905) Report of Mr. Alvin Seale of the United States Fish Commission on the introduction of top-minnows to Hawaii from Galvenston. Texas Hawn. For Agric 364–367

  • Seale A (1917) The mosquito fish, Gambusia affinis (Baird and Girard) in the Philippine Islands. Philipp J Sci 12:177–189

    Google Scholar 

  • Stearns SC (1983) The genetic basis of differences in life-history traits among six populations of mosquitofish (Gambusia affinis) that shared ancestors in 1905. Evolution 37:618–627

    Article  Google Scholar 

  • Stockwell CA, Weeks SC (1999) Translocations and rapid evolutionary responses in recently established populations of western mosquitofish (Gambusia affinis). Animal Conserv 2:103–110

    Article  Google Scholar 

  • Stockwell CA, Mulvey M, Vinyard GL (1996) Translocations and the preservation of allelic diversity. Conserv Biol 10:1133–1141

    Article  Google Scholar 

  • Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155

    PubMed  CAS  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2001) Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and the source of introduced populations. Mol Ecol 10:2151–2161

    Article  PubMed  CAS  Google Scholar 

  • Van Dine DL (1907) The Introduction of topminnows (natural enemies of mosquitoes) into the Hawaiian Islands. Hawaii agricultural Experiment station.

  • Vidal O, García-Berthou E, Tedesco PA, García-Marín J-L (2009) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions 12:841–851

    Article  Google Scholar 

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Acknowledgments

We would like to thank K. Scribner for providing information on site locations. This work was supported by funds from the NDSU, Environmental and Conservation Sciences Graduate Program Postdoctoral Fellowship awarded to KP and North Dakota EPSCoR and National Science Foundation Grant EPS-0814442 to CAS. Additional funding from a NDSU President’s Travel Grant supported CAS during sampling in New Zealand. Specimen handling and collection was conducted under North Dakota State University IACUC #A0902, and with the assistance of S. Martin and J. Terfehr.

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Correspondence to C. A. Stockwell.

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Purcell, K.M., Ling, N. & Stockwell, C.A. Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biol Invasions 14, 2057–2065 (2012). https://doi.org/10.1007/s10530-012-0213-1

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