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Comparative phylogeography of invasive Rattus rattus and Rattus norvegicus in the U.S. reveals distinct colonization histories and dispersal

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Abstract

Invasive Rattus are arguably the most costly and destructive invasive species on the planet, but little is known concerning their invasion history and population structure in the U.S. We utilized both nuclear microsatellites and mitochondrial DNA sequences (mtDNA) to compare the colonization history, patterns of gene flow, and levels of genetic diversity of Rattus rattus and R. norvegicus in the U.S. Analyses of mtDNA suggest R. rattus is characterized by a single rapid expansion into the U.S. from one or two very closely related mtDNA lineages or geographic sources. For R. norvegicus, mtDNA analyses suggest at least four invasions distinct in space and/or time have occurred to establish its distribution in the U.S. Microsatellite analyses suggest for R. rattus that dispersal is characterized by an isolation-by-distance pattern, suggesting a relatively low frequency of long distance dispersal, and low levels of establishment for novel propagules. In contrast, microsatellite analyses of R. norvegicus suggest high frequencies of long distance dispersal and essentially panmixia among nearly all sampled populations, as well as a high frequency of novel propagules entering at the east and west coasts and assimilating into established populations. We discuss these results in the context of invasive Rattus management in the U.S. and their implications for invasive species in general, as well as the implications for managing the spread of rat-borne pathogens.

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References

  • Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518

    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 

  • Aplin KP, Chesser T, ten Have J (2003) Evolutionary biology of the genus Rattus: profile of an archetypal rodent pest. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) Rats, mice, and people: rodent biology and management. The Australian Centre for International Agricultural Research (ACIAR), Canberra, pp 487–498

    Google Scholar 

  • Aplin KP, Suzuki H, Chinen AA et al (2011) Multiple genetic origins of commensalism and complex dispersal history of black rats. PLoS ONE 6:e26357

    Article  PubMed  CAS  Google Scholar 

  • Armitage PL (1993) Commensal rats in the New World, 1492–1992. Biologist 40:174–178

    Google Scholar 

  • Bastos AD, Nair D, Taylor PJ et al (2011) Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa. BMC Genet 12:26

    Article  PubMed  Google Scholar 

  • Biek R, Real LA (2010) The landscape genetics of infectious disease emergence and spread. Mol Ecol 19:3515–3531

    Article  PubMed  Google Scholar 

  • Breed AC, Field HE, Smith CS, Edmonston J, Meers J (2010) Bats without borders: long-distance movements and implications for disease risk management. EcoHealth 7:204–212

    Article  PubMed  Google Scholar 

  • Caire W, Tyler JD, Glass BP, Mares MA (1989) Mammals of Oklahoma. University of Oklahoma Press, Norman, OK

    Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Conroy CJ, Rowe KC, Rowe KMC, Kamath PL, Aplin KP, Lucia H, James DK, Moritz C, Patton JL (2012) Cryptic genetic diversity in Rattus of the San Francisco Bay region, California. Biol Invasions. doi:10.1007/s10530-012-0323-9

  • Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impacts, control, and control impact. Biol Rev 78:347–383

    Article  PubMed  Google Scholar 

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Res 10:556–557

    Article  Google Scholar 

  • Cullingham CI, Kyle CJ, Pond BA, Rees EE, White BN (2009) Differential permeability of rivers to raccoon gene flow corresponds to rabies incidence in Ontario, Canada. Mol Ecol 19:3592–3602

    Google Scholar 

  • Drummond AJ, Ashton B, Cheung M et al (2010) Geneious, version 5.0. http://www.geneious.com

  • Ecke DH (1954) An invasion of Norway rats in southwest Georgia. J Mamm 35:521–525

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2010) Interspecific competitive interactions between Rattus norvegicus and R. rattus. Unpublished Thesis. University of Waikato, New Zealand

  • Frankham R, Ralls K (1998) Conservation biology: inbreeding leads to extinction. Nature 392:441–442

    Article  CAS  Google Scholar 

  • Frittelli JF, Lee MR, Medalia J, O’Rourke R, Perl R (2005) Port and maritime security: background and issues for congress. Novinka Books, New York City, NY

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 133:693–709

    Google Scholar 

  • Galimand M (1997) Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N Engl J Med 337:677–680

    Article  PubMed  CAS  Google Scholar 

  • Gibbs MJ, Armstrong JS, Gibbs AJ (2001) Recombination in the hemagglutinin gene of the 1918 “Spanish flu”. Science 293:1842–1845

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Department of Ecology and Evolution, University of Lausanne, Switzerland. Available at: http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 10 January 2012

  • Gratz NG (1984) The global public health importance of rodents. In: Dubock AC (ed) Proceedings of a conference on the organization and practice of vertebrate pest control. World Health Organization, Geneva, Switzerland, pp 413–435

    Google Scholar 

  • Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC (2001) Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294:161–165

    Article  PubMed  CAS  Google Scholar 

  • Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation. Heredity 104:88–99

    Article  PubMed  CAS  Google Scholar 

  • He CQ, Xie ZX, Han GZ et al (2009) Homologous recombination as an evolutionary force in the avian influenza A virus. Mol Biol Evol 26:177–187

    Article  PubMed  CAS  Google Scholar 

  • Hingston M, Goodman SM, Ganzhorn JU, Sommer S (2005) Reconstruction of the colonization of southern Madagascar by Rattus rattus. J Biogeogr 32:1549–1559

    Article  Google Scholar 

  • Holmes EC (2008) Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol 62:307–328

    Article  PubMed  CAS  Google Scholar 

  • Howald G, Donlan CJ, Galvan JP et al (2007) Invasive rodent eradication on islands. Conserv Biodiv 21:1258–1268

    Google Scholar 

  • Inglesby TV, Dennis DT, Henderson DA et al (2000) Plague as a biological weapon. J Am Med Assoc 283:2281–2290

    Article  CAS  Google Scholar 

  • Island Conservation (2006) Evaluation of primary and secondary exposure risks to land bird species for: experimental use permit application for field efficacy trial of 0.0025% brodifacoum broadcast bait to eradicate introduced rats from Aleutian Islands in the Alaska Maritime National Wildlife Refuge, July 20, 2006. Island Conservation, Center for Ocean Health, Santa Cruz, CA

  • Jackson WB (1982) Norway rat and allies. In: Chapman JA, Feldhammer GA (eds) Wild Mammals of North America. Johns Hopkins University Press, Baltimore, MD, pp 1077–1088

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) Clumpp a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Kaluza P, Kolzsch GastnerMT, Blasius B (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103

    Article  PubMed  Google Scholar 

  • Keeling MJ, Gilligan CA (2000) Metapopulation dynamics of bubonic plague. Nature 407:903–906

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1953) “Stepping-stone” model of population. Annu Rep Natl Inst Genet Jpn 3:62–63

    Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR, 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 

  • Kolbe JJ, Larson A, Losos JB, de Queiroz K (2008) Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biol Lett 4:434–437

    Article  PubMed  Google Scholar 

  • Lack JB, Greene DU, Conroy CJ, Hamilton MJ, Braun JK, Mares MA, Van Den Bussche RA (2012) Invasion facilitates hybridization with introgression with introgression in the Rattus rattus species complex. Mol Ecol 21:3545–3561

    Google Scholar 

  • Landon DB (1991) Zooarchaeology and urban foodways: a case study from eastern Massachusetts. Unpublished Dissertation, Boston University

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • MacGillivray W (1838) A history of British quadrupeds. WH Lizars, Edinburgh, Scotland

    Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Inc., Sunderland, Massachusetts

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Martel C, Viard F, Bourguet D, Garcia-Meunier P (2004) Invasion by the marine gastropod Ocinebrellus orinata in France I. Scenario for the source of introduction. J Exp Mar Biol Ecol 305:155–170

    Article  Google Scholar 

  • Matisoo-Smith E, Robins JH (2004) Origins and dispersals of Pacific people: evidence from mtDNA phylogenies of the Pacific rat. Proc Natl Acad Sci USA 101:9167–9172

    Article  PubMed  CAS  Google Scholar 

  • Matisoo-Smith E, Roberts RM, Irwin GJ, Allen JS, Penny D, Lambert DM (1998) Patterns of prehistoric human mobility in Polynesia indicated by mtDNA from the Pacific rat. Proc Natl Acad Sci USA 95:15145–15150

    Article  PubMed  CAS  Google Scholar 

  • Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270

    Article  PubMed  Google Scholar 

  • Musser GG, Carleton MD (2005) Family Muridae. In: Wilson DE, Reeder DM (eds) Mammal species of the world, a taxonomic and geographic reference. Smithsonian Institute Press, Washington, DC, pp 1189–1531

    Google Scholar 

  • Novak SJ, Mack RN (2001) Tracing plant introduction and spread: genetic evidence from Bromus tectorum (cheatgrass). Bioscience 51:114–122

    Article  Google Scholar 

  • Nowak R (1999) Walker’s Mammals of the world, 6th edn. John’s Hopkins University Press, Baltimore, Maryland

    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 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Ecol Evol 13:288–294

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Robertson BC, Gimmell NJ (2004) Defining eradication units in pest control progammes. J Appl Ecol 41:1032–1041

    Article  Google Scholar 

  • Robins JH, Hingston M, Matisoo-Smith E, Ross HA (2007) Identifying Rattus species using mitochondrial DNA. Mol Ecol Notes 7:717–729

    Article  CAS  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 14:4299–4312

    Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP. DNA polymorphism analyses by coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ruffina L, Vidal E (2010) Early colonization of Mediterranean islands by Rattus rattus: a review of zooarcheological data. Biol Invasions 12:2389–2394

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schwartz CW, Schwartz ER (1981) The wild mammals of Missouri. University of Missouri Press, Columbia, MO

    Google Scholar 

  • Silver J (1927) The introduction and spread of house rats in the United States. J Mamm 8:58–60

    Google Scholar 

  • Simberloff D (2009) We can eliminate invasions or live with them. Successful management projects. Biol Invasions 11:149–157

    Article  Google Scholar 

  • Skellman JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218

    Google Scholar 

  • Suarez AV, Holoway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100

    Article  PubMed  CAS  Google Scholar 

  • Sullivan R (2004) Rats: observations on the history and habitat of the city’s most unwanted inhabitants. Bloomsbury Publishing, New York City, NY

    Google Scholar 

  • Tollenaere C, Brouat C, Duplantier JM et al (2010) Phylogeography of the introduced species Rattus rattus in the western Indian Ocean, with special emphasis on the colonization history of Madagascar. J Biogeogr 37:398–410

    Article  Google Scholar 

  • Twigg G (1975) The brown rat. David and Charles, London

    Google Scholar 

  • Urdaneta-Marquez L, Failloux AB (2010) Population genetic structure of Aedes aegypti, of the principle vector of dengue viruses. Infect Genet Evol 11:253–261

    Article  PubMed  Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associate, Inc., Sunderland, MA

    Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  Google Scholar 

  • Wilson AB, Naish KA, Boulding EG (1999) Multiple dispersal strategies of the invasive quagga mussel (Dreissena bugensis) as revealed by microsatellite analysis. Can J Fish Aquat Species 56:2248–2261

    Article  Google Scholar 

  • Witmer GW, Boyd F, Hillis-Star Z (2007) The successful eradication of introduced roof rats (Rattus rattus) from Buck Island using diphacinone, followed by an irruption of house mice (Mus musculus). Wildl Res 34:108–115

    Article  CAS  Google Scholar 

  • Yom-Tov Y, Yom-Tov S, Moller H (1999) Competition, coexistence, and adaptation amongst rodent invaders to Pacific and New Zealand Islands. J Biogeography 26:947–958

    Article  Google Scholar 

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Lack, J.B., Hamilton, M.J., Braun, J.K. et al. Comparative phylogeography of invasive Rattus rattus and Rattus norvegicus in the U.S. reveals distinct colonization histories and dispersal. Biol Invasions 15, 1067–1087 (2013). https://doi.org/10.1007/s10530-012-0351-5

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