Biological Invasions

, Volume 15, Issue 5, pp 1067–1087 | Cite as

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

  • Justin B. Lack
  • Meredith J. Hamilton
  • Janet K. Braun
  • Michael A. Mares
  • Ronald A. Van Den Bussche
Original Paper


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.


Rattus rattus Rattus norvegicus Colonization history Interspecific interaction Dispersal 

Supplementary material

10530_2012_351_MOESM1_ESM.eps (645 kb)
Supplementary material 1 (EPS 644 kb)
10530_2012_351_MOESM2_ESM.eps (654 kb)
Supplementary material 2 (EPS 654 kb)
10530_2012_351_MOESM3_ESM.docx (204 kb)
Supplementary material 3 (DOCX 203 kb)
10530_2012_351_MOESM4_ESM.docx (92 kb)
Supplementary material 4 (DOCX 91 kb)
10530_2012_351_MOESM5_ESM.docx (86 kb)
Supplementary material 5 (DOCX 86 kb)


  1. 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 19:1509–1518CrossRefGoogle Scholar
  2. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  3. 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 487–498Google Scholar
  4. Aplin KP, Suzuki H, Chinen AA et al (2011) Multiple genetic origins of commensalism and complex dispersal history of black rats. PLoS ONE 6:e26357PubMedCrossRefGoogle Scholar
  5. Armitage PL (1993) Commensal rats in the New World, 1492–1992. Biologist 40:174–178Google Scholar
  6. 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 12:26PubMedCrossRefGoogle Scholar
  7. Biek R, Real LA (2010) The landscape genetics of infectious disease emergence and spread. Mol Ecol 19:3515–3531PubMedCrossRefGoogle Scholar
  8. Breed AC, Field HE, Smith CS, Edmonston J, Meers J (2010) Bats without borders: long-distance movements and implications for disease risk management. EcoHealth 7:204–212PubMedCrossRefGoogle Scholar
  9. Caire W, Tyler JD, Glass BP, Mares MA (1989) Mammals of Oklahoma. University of Oklahoma Press, Norman, OKGoogle Scholar
  10. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  11. 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
  12. Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impacts, control, and control impact. Biol Rev 78:347–383PubMedCrossRefGoogle Scholar
  13. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Res 10:556–557CrossRefGoogle Scholar
  14. 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 19:3592–3602Google Scholar
  15. Drummond AJ, Ashton B, Cheung M et al (2010) Geneious, version 5.0.
  16. Ecke DH (1954) An invasion of Norway rats in southwest Georgia. J Mamm 35:521–525CrossRefGoogle Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  18. Foster SP (2010) Interspecific competitive interactions between Rattus norvegicus and R. rattus. Unpublished Thesis. University of Waikato, New ZealandGoogle Scholar
  19. Frankham R, Ralls K (1998) Conservation biology: inbreeding leads to extinction. Nature 392:441–442CrossRefGoogle Scholar
  20. 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, NYGoogle Scholar
  21. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 133:693–709Google Scholar
  22. Galimand M (1997) Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N Engl J Med 337:677–680PubMedCrossRefGoogle Scholar
  23. Gibbs MJ, Armstrong JS, Gibbs AJ (2001) Recombination in the hemagglutinin gene of the 1918 “Spanish flu”. Science 293:1842–1845PubMedCrossRefGoogle Scholar
  24. 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: Accessed 10 January 2012
  25. 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 413–435Google Scholar
  26. 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 294:161–165PubMedCrossRefGoogle Scholar
  27. Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation. Heredity 104:88–99PubMedCrossRefGoogle Scholar
  28. He CQ, Xie ZX, Han GZ et al (2009) Homologous recombination as an evolutionary force in the avian influenza A virus. Mol Biol Evol 26:177–187PubMedCrossRefGoogle Scholar
  29. Hingston M, Goodman SM, Ganzhorn JU, Sommer S (2005) Reconstruction of the colonization of southern Madagascar by Rattus rattus. J Biogeogr 32:1549–1559CrossRefGoogle Scholar
  30. Holmes EC (2008) Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol 62:307–328PubMedCrossRefGoogle Scholar
  31. Howald G, Donlan CJ, Galvan JP et al (2007) Invasive rodent eradication on islands. Conserv Biodiv 21:1258–1268Google Scholar
  32. Inglesby TV, Dennis DT, Henderson DA et al (2000) Plague as a biological weapon. J Am Med Assoc 283:2281–2290CrossRefGoogle Scholar
  33. 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, CAGoogle Scholar
  34. 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 1077–1088Google Scholar
  35. 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 23:1801–1806PubMedCrossRefGoogle Scholar
  36. Kaluza P, Kolzsch GastnerMT, Blasius B (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103PubMedCrossRefGoogle Scholar
  37. Keeling MJ, Gilligan CA (2000) Metapopulation dynamics of bubonic plague. Nature 407:903–906PubMedCrossRefGoogle Scholar
  38. Kimura M (1953) “Stepping-stone” model of population. Annu Rep Natl Inst Genet Jpn 3:62–63Google Scholar
  39. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  40. 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 4:434–437PubMedCrossRefGoogle Scholar
  41. 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 21:3545–3561Google Scholar
  42. Landon DB (1991) Zooarchaeology and urban foodways: a case study from eastern Massachusetts. Unpublished Dissertation, Boston UniversityGoogle Scholar
  43. 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 154:1–17CrossRefGoogle Scholar
  44. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  45. MacGillivray W (1838) A history of British quadrupeds. WH Lizars, Edinburgh, ScotlandGoogle Scholar
  46. Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Inc., Sunderland, MassachusettsGoogle Scholar
  47. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  48. 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 305:155–170CrossRefGoogle Scholar
  49. 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 101:9167–9172PubMedCrossRefGoogle Scholar
  50. 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 95:15145–15150PubMedCrossRefGoogle Scholar
  51. Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270PubMedCrossRefGoogle Scholar
  52. 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 1189–1531Google Scholar
  53. Novak SJ, Mack RN (2001) Tracing plant introduction and spread: genetic evidence from Bromus tectorum (cheatgrass). Bioscience 51:114–122CrossRefGoogle Scholar
  54. Nowak R (1999) Walker’s Mammals of the world, 6th edn. John’s Hopkins University Press, Baltimore, MarylandGoogle Scholar
  55. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  56. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  57. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Ecol Evol 13:288–294Google Scholar
  58. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  59. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  60. Robertson BC, Gimmell NJ (2004) Defining eradication units in pest control progammes. J Appl Ecol 41:1032–1041CrossRefGoogle Scholar
  61. Robins JH, Hingston M, Matisoo-Smith E, Ross HA (2007) Identifying Rattus species using mitochondrial DNA. Mol Ecol Notes 7:717–729CrossRefGoogle Scholar
  62. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  63. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 14:4299–4312Google Scholar
  64. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP. DNA polymorphism analyses by coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  65. Ruffina L, Vidal E (2010) Early colonization of Mediterranean islands by Rattus rattus: a review of zooarcheological data. Biol Invasions 12:2389–2394CrossRefGoogle Scholar
  66. Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  67. Schwartz CW, Schwartz ER (1981) The wild mammals of Missouri. University of Missouri Press, Columbia, MOGoogle Scholar
  68. Silver J (1927) The introduction and spread of house rats in the United States. J Mamm 8:58–60Google Scholar
  69. Simberloff D (2009) We can eliminate invasions or live with them. Successful management projects. Biol Invasions 11:149–157CrossRefGoogle Scholar
  70. Skellman JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218Google Scholar
  71. 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 98:1095–1100PubMedCrossRefGoogle Scholar
  72. Sullivan R (2004) Rats: observations on the history and habitat of the city’s most unwanted inhabitants. Bloomsbury Publishing, New York City, NYGoogle Scholar
  73. 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 37:398–410CrossRefGoogle Scholar
  74. Twigg G (1975) The brown rat. David and Charles, LondonGoogle Scholar
  75. Urdaneta-Marquez L, Failloux AB (2010) Population genetic structure of Aedes aegypti, of the principle vector of dengue viruses. Infect Genet Evol 11:253–261PubMedCrossRefGoogle Scholar
  76. Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associate, Inc., Sunderland, MAGoogle Scholar
  77. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedGoogle Scholar
  78. 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 56:2248–2261CrossRefGoogle Scholar
  79. 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 34:108–115CrossRefGoogle Scholar
  80. Yom-Tov Y, Yom-Tov S, Moller H (1999) Competition, coexistence, and adaptation amongst rodent invaders to Pacific and New Zealand Islands. J Biogeography 26:947–958CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Justin B. Lack
    • 1
    • 4
  • Meredith J. Hamilton
    • 1
  • Janet K. Braun
    • 2
  • Michael A. Mares
    • 2
    • 3
  • Ronald A. Van Den Bussche
    • 1
  1. 1.Department of ZoologyOklahoma State UniversityStillwaterUSA
  2. 2.Sam Noble MuseumUniversity of OklahomaNormanUSA
  3. 3.Department of ZoologyUniversity of OklahomaNormanUSA
  4. 4.Department of ZoologyOklahoma State UniversityStillwaterUSA

Personalised recommendations