Abstract
The efficacy of invasive species management is dependent on a thorough understanding of the size, origin, and genetic structure of invasive populations. We evaluated the genetic diversity and structure of the western mosquitofish, Gambusia affinis, across the North Island of New Zealand in an effort to better understand the genetic structure and post-introduction dispersal mechanisms of this highly invasive estuarine species. We found clear evidence of founder effects and significant genetic structure for populations derived from populations initially established in New Zealand in the 1930s. Our findings indicate that G. affinis populations have succeeded through a combination of localized dispersal and human-assisted colonization. Additionally, we identify a series of populations in one region that are apparently genetically isolated from the other regions. This area could thus represent a “significant eradication unit” where re-colonization is unlikely. Our results highlight the utility and value of molecular tools as an efficient method to facilitate a richer understanding of the nature and condition of invasive species while identifying definitive management objectives.
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References
Alemadi S, Jenkins D (2008) Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae). Biol Invasions 10:59–66. doi:10.1007/s10530-007-9109-x
Ayres RM, Pettigrove VJ, Hoffmann AA (2010) 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. doi:10.1007/s10530-010-9766-z
Ayres RM, Pettigrove VJ, Hoffmann AA (2012) Genetic structure and diversity of introduced eastern mosquitofish (Gambusia holbrooki) in south-eastern Australia. Mar Freshw Res 63:1206. doi:10.1071/MF11279
Blanchet S (2012) The use of molecular tools in invasion biology: an emphasis on freshwater ecosystems. Fisher Manag Ecol 19:120–132. doi:10.1111/j.1365-2400.2011.00832.x
Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002–1015. doi:10.1111/j.0014-3820.2001.tb00617.x
Brown KL (1985) Demographic and genetic characteristics of dispersal in the Mosquitofish, Gambusia affinis (Pisces: Poeciliidae). Copeia 1985:597–612. doi:10.2307/1444750
Congdon BC (1994) Characteristics of dispersal in the eastern mosquitofish Gambusia holbrooki. J Fish Biol 45:943–952. doi:10.1111/j.1095-8649.1994.tb01064.x
Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374
Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539. doi:10.1186/1471-2105-9-539
Cote J, Fogarty S, Weinersmith K et al (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc Biol Sci 277:1571–1579. doi:10.1098/rspb.2009.2128
Díez-del-Molino D, Carmona-Catot G, Araguas R-M et al (2013) Gene flow and maintenance of genetic diversity in invasive mosquitofish (Gambusia holbrooki). PLoS ONE 8:e82501. doi:10.1371/journal.pone.0082501
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. doi:10.1111/j.1365-294X.2007.03538.x
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genet Resour 4:359–361
Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Reconstructing routes of invasion. Mol Ecol 19:4113–4130. doi:10.1111/j.1365-294X.2010.04773.x
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. doi:10.1111/j.1365-294X.2005.02553.x
Everman E, Klawinski P (2013) Human-facilitated jump dispersal of a non-native frog species on Hawai’i Island. J Biogeogr 40:1961–1970. doi:10.1111/jbi.12146
Faubet P, Waples R, Gaggiotti O (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166
Fraser EJ, Macdonald DW, Oliver MK et al (2013) Using population genetic structure of an invasive mammal to target control efforts—an example of the American mink in Scotland. Biol Conserv 167:35–42. doi:10.1016/j.biocon.2013.07.011
Gilbert KJ, Andrew RL, Bock DG et al (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure. Mol Ecol 21:4925–4930
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grapputo A, Bisazza A, Pilastro A (2006) Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbrooki). Itali J Zool 73:67–73. doi:10.1080/11250000500502111
Krumholz LA (1948) Reproduction in the Western mosquitofish, Gambusia affinis affinis (Baird & Girard), and Its Use in Mosquito Control. Ecol Monogr 18:1. doi:10.2307/1948627
LaRue E, Ruetz C, Stacey M, Thum R (2011) Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species. Hydrobiologia 663:71–82. doi:10.1007/s10750-010-0555-6
Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (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. doi:10.1007/s10592-005-9098-1
Le Roux J, Wieczorek AM (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17. doi:10.1111/j.1744-7348.2008.00280.x
Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449. doi:10.1046/j.1365-294X.2002.01612.x
Lindholm AK, Breden F, Alexander HJ (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682. doi:10.1111/j.1365-294X.2005.02697.x
Ling N (2004) Gambusia in New Zealand: really bad or just misunderstood? N Z J Mar Freshw Res 38:473–480. doi:10.1080/00288330.2004.9517254
McDowall RM (1990) New Zealand freshwater fishes: a natural history and guide, revised. MAF Pub. Group
Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour. doi:10.1111/1755-0998.12216
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. doi:10.1111/j.1471-8286.2004.00684.x
Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16. doi:10.1016/j.tree.2006.09.003
Peacock MM, Beard KH, O’neill EM (2009) Strong founder effects and low genetic diversity in introduced populations of Coqui frogs. Mol Ecol 18:3603–3615. doi:10.1111/j.1365-294X.2009.04308.x
Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
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. doi:10.1007/s12686-010-9362-7
Purcell KM, Ling N, Stockwell CA (2012) Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biol Invasions 14:2057–2065. doi:10.1007/s10530-012-0213-1
Pyke G (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15:339–365. doi:10.1007/s11160-006-6394-x
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. doi:10.1146/annurev.ecolsys.39.110707.173451
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reddy SR, Pandian TJ (1974) Effect of running water on the predatory efficiency of the larvivorous fish Gambusia affinis. Oecologia 16:253–256. doi:10.1007/BF00345887
Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia Species. Biol Invasions 6:379–391. doi:10.1023/B:BINV.0000034618.93140.a5
Rehage JS, Barnett BK, Sih A (2005) Foraging behavior and invasiveness: do invasive Gambusia exhibit higher feeding rates and broader diets than their noninvasive relatives? Ecol Freshw Fish 14:352–360. doi:10.1111/j.1600-0633.2005.00109.x
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. doi:10.2307/2409177
Rollins LA, Woolnough AP, Wilton AN (2009) Invasive species can’t cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol Ecol 18:1560–1573. doi:10.1111/j.1365-294X.2009.04132.x
Rollins LA, Moles AT, Lam S et al (2013) High genetic diversity is not essential for successful introduction. Ecol Evol. doi:10.1002/ece3.824
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x
Ruiz-Navarro A, Verdiell-Cubedo D, Torralva M, Oliva-Paterna FJ (2013) Removal control of the highly invasive fish Gambusia holbrooki and effects on its population biology: learning by doing. Wildl Res 40:82–89
Sanz N, Araguas RM, Vidal O, et al. (2013) Genetic characterization of the invasive mosquitofish (Gambusia spp.) introduced to Europe: population structure and colonization routes. Biol Invasions. doi:10.1007/s10530-013-0456-5
Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33. doi:10.1016/j.tree.2006.08.009
Seale A (1917) The mosquito fish, Gambusia affinis (Baird and Girard) in the Philippine Islands. Philipp J Sci 12:177–189
Stockwell CA, Henkanaththegedara SM (2011) Evolutionary conservation biology. Ecology and evolution of Poeciliid fishes. University of Chicago Press, Chicago, p 424
Stockwell CA, Weeks SC (1999) Translocations and rapid evolutionary responses in recently established populations of western mosquitofish (Gambusia affinis). Anim Conservation 2:103–110. doi:10.1111/j.1469-1795.1999.tb00055.x
Stockwell CA, Mulvey M, Vinyard GL (1996) Translocations and the preservation of allelic diversity. Conservation Biol 10:1133–1141
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 P, García-Marín J-L (2010) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions 12:841–851
Vidal O, Sanz N, Araguas R-M et al (2012) SNP diversity in introduced populations of the invasive Gambusia holbrooki. Ecol Freshw Fish 21:100–108
Vitule JRS, Freire CA, Simberloff D (2009) Introduction of non-native freshwater fish can certainly be bad. Fish Fish 10:98–108. doi:10.1111/j.1467-2979.2008.00312.x
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi:10.2307/2408641
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163(3):1177–1191
Acknowledgments
We thank Nick Ling for introducing us to this study system and identifying some of the collection sites. We also thank Brandon Kowalski for providing many of the samples used in these analyses, and we thank Makenzie Stockwell, Jan Terfehr and Monica Gruber for assistance in collecting mosquitofish. We also thank Pete Ritchie for logistical assistance and two anonymous reviewers for valuable insights on this manuscript. This work was supported by funds from the NDSU, Environmental and Conservation Sciences Graduate Program Postdoctoral Fellowship to KP, a NDSU Centennial Grant award to CAS and a North Dakota EPSCoR and National Science Foundation Grant EPS-0814442 to CAS. Additional funds from a NDSU President’s Travel Grant, and from the NDSU College of Science and Mathematics supported CAS during field collections.
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Purcell, K.M., Stockwell, C.A. An evaluation of the genetic structure and post-introduction dispersal of a non-native invasive fish to the North Island of New Zealand. Biol Invasions 17, 625–636 (2015). https://doi.org/10.1007/s10530-014-0753-7
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DOI: https://doi.org/10.1007/s10530-014-0753-7