Biological Invasions

, Volume 20, Issue 11, pp 3207–3226 | Cite as

Introduction history and genetic diversity of the invasive ant Solenopsis geminata in the Galápagos Islands

  • Nina Wauters
  • Wouter Dekoninck
  • Denis Fournier
Original Paper


The Galápagos Islands constitute one of the most pristine tropical systems on Earth. However, the complex and fragile equilibrium of native species is threatened by invasive species, among which is one of the most successful ants in the world, the tropical fire ant, Solenopsis geminata. We characterized the genetic structure and diversity of populations of S. geminata in the Galápagos Islands and unravelled the archipelago colonization by combining Bayesian clustering methods and coalescent-based scenario testing. Using 12 microsatellite markers and one mitochondrial DNA fragment (COI), we analysed individuals collected in all main invaded islands of the archipelago and from the native areas in Costa Rica and mainland Ecuador. We also used mitochondrial DNA to infer evolutionary relationships of samples collected in Galápagos Islands, Ecuador, Costa Rica and other Latin American countries. Our results showed that genetic diversity was significantly lower in Galápagos Islands and mainland Ecuador populations when compared to Costa Rican populations, and that samples from Galápagos Islands and mainland Ecuador (Guayaquil) clustered in a single group and all share a single mtDNA haplotype. Approximate Bayesian Computation favoured a scenario assuming that populations from Galápagos Islands diverged from mainland Ecuador. The city of Guyaquil, an obligatory hub for tourism and trade, could act as a bridgehead.


Approximate Bayesian Computation Biological invasions Founder effect Island colonization Microsatellites 



We are grateful to M. Martin Cerezo for her help in genotyping, J. Kwasigroch for his assisting during the process of data simulation, J. Parikka for his reading of the first draft of this manuscript and H.J. Axen, J. Foucaud, D. Gotzek, T. Guillemaud, F. Hendrickx, E. Lombaert and anonymous referees for their useful comments on a previous version of this paper. This work was supported by several grants from the Belgian FRS-FNRS (Fonds National pour la Recherche Scientifique) (DF), the Fonds Defay (DF), the Royal Belgian Institute of Natural Sciences (WD) and the King Léopold III Fund (WD). We are also grateful to Gontran Sonet (RBINS) for his help preparing and calibrating the sequencer. The molecular research was funded by the FWO project (G0D2915N)—Poneroid Ants of Ecuador (Formicidae: Agroecomyrmicinae, Amblyoponinae, Ponerinae, Proceratiinae, Paraponerinae). All administration on legislation and permits was done with the help of Henri Herrera and Sonia Cisneros of the Charles Darwin Foundation in collaboration with the Galapagos National Park Directorate (GNPD). This publication is contribution number 2195 of the Charles Darwin Foundation for the Galápagos Islands.

Author contributions

D.F. designed the study. All authors collected samples. N.W. performed the molecular work. N.W. and D.F. analysed the data. N.W. and D.F. wrote the manuscript with input from W.D.

Supplementary material

10530_2018_1769_MOESM1_ESM.docx (2.8 mb)
Supplementary material 1 (DOCX 2843 kb)
10530_2018_1769_MOESM2_ESM.xlsx (35 kb)
Supplementary material 2 (XLSX 34 kb)
10530_2018_1769_MOESM3_ESM.pdf (36 kb)
Supplementary material 3 (PDF 35 kb)
10530_2018_1769_MOESM4_ESM.pdf (1.1 mb)
Supplementary material 4 (PDF 1160 kb)
10530_2018_1769_MOESM5_ESM.pdf (739 kb)
Supplementary material 5 (PDF 738 kb)
10530_2018_1769_MOESM6_ESM.jpg (2.2 mb)
Supplementary material 6 (JPEG 2246 kb)
10530_2018_1769_MOESM7_ESM.jpg (2.1 mb)
Supplementary material 7 (JPEG 2136 kb)


  1. Adams CT, Banks WA, Plumley JK (1976) Polygyny in the tropical fire ant Solenopsis geminata with notes on the imported fire ant Solenopsis invicta. Fla Entomol 59:411–415. CrossRefGoogle Scholar
  2. Ascunce MS, Bouwma AM, Shoemaker D (2009) Characterization of 24 microsatellite markers in 11 species of fire ants in the genus Solenopsis (Hymenoptera: Formicidae). Mol Ecol Resour 9:1475–1479. CrossRefPubMedGoogle Scholar
  3. Ascunce MS et al (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068. CrossRefPubMedGoogle Scholar
  4. Asigau S, Hartman DA, Higashiguchi JM, Parker PG (2017) The distribution of mosquitoes across an altitudinal gradient in the Galapagos Islands. J Vector Ecol 42:243–253CrossRefGoogle Scholar
  5. Auger-Rozenberg MA, Boivin T, Magnoux E, Courtin C, Roques A, Kerdelhué C (2012) Inferences on population history of a seed chalcid wasp: invasion success despite a severe founder effect from an unexpected source population. Mol Ecol 21:6086–6103. CrossRefPubMedGoogle Scholar
  6. Barrès B, Carlier J, Seguin M, Fenouillet C, Cilas C, Ravigné V (2012) Understanding the recent colonization history of a plant pathogenic fungus using population genetic tools and Approximate Bayesian Computation. Heredity 109:269–279. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bataille A et al (2009) Evidence for regular ongoing introductions of mosquito disease vectors into the Galápagos Islands. Proc Biol Sci 276:3769–3775. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Beaumont M (2010) Approximate Bayesian computation in evolution and ecology. Annu Rev Ecol Evol Syst 41:379–406. CrossRefGoogle Scholar
  9. Beaumont MA, Zhang W, Balding DJ (2002) Approximate bayesian computation in population genetics. Genetics 162:2025–2035PubMedPubMedCentralGoogle Scholar
  10. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1998) Genetix, logiciel sous WindowsTM pour la génétique des populations, 3.0 edn. Laboratoire Génome et Populations, CNRS UPR 9060, Université de Montpellier II, Montpellier (France). doi:Windows 3.1 ou ultérieurGoogle Scholar
  11. Bermond G et al (2012) Secondary contact and admixture between independently invading populations of the western corn rootworm, Diabrotica virgifera virgifera in Europe. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bigue M, Rosero O, Bewington L, Cervantes K (2012) The quarantine chain—establishing an effective biosecurity system to prevent the introduction of invasive species into the Galápagos Islands. WildAid, San Francisco, CaliforniaGoogle Scholar
  13. Boissin E et al (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744. CrossRefPubMedGoogle Scholar
  14. Bolfíková B, Konečný A, Pfäffle M, Skuballa J, Hulva P (2013) Population biology of establishment in New Zealand hedgehogs inferred from genetic and historical data: conflict or compromise? Mol Ecol 22:3709–3720. CrossRefPubMedGoogle Scholar
  15. Brandão CRF, Paiva RVS (1994) The Galapagos ant fauna and the attributes of colonizing ant species. In: Williams DF (ed) Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, pp 1–10Google Scholar
  16. Brouat C et al (2014) Invasion genetics of a human commensal rodent: the black rat Rattus rattus in Madagascar. Mol Ecol 23:4153–4167. CrossRefPubMedGoogle Scholar
  17. Carroll SP (2011) Conciliation biology: the eco-evolutionary management of permanently invaded biotic systems. Evol Appl 4:184–199. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Causton CE, Peck SB, Sinclair BJ, Roque-Albelo L, Hodgson CJ, Landry B (2006) Alien insects: threats and implications for conservation of Galápagos Islands. Ann Entomol Soc Am 99:121–143.[0121:AITAIF]2.0.CO;2 CrossRefGoogle Scholar
  19. Chang V, Ota AK (1990) Ant control in Hawaiian drip irrigation systems. In: Vander Meer RK, Jaffe K, Cedeno A (eds) Applied myrmecology: a world perspective. Westview Press, Boulder, pp 708–715Google Scholar
  20. Cornuet J-M, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinform 11:401. CrossRefGoogle Scholar
  21. Cornuet J-M et al (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189. CrossRefPubMedGoogle Scholar
  22. Davis MA (2009) Invasion biology. Oxford University Press, OxfordGoogle Scholar
  23. 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. CrossRefPubMedGoogle Scholar
  24. Dudaniec RY, Gardner MG, Donnellan S, Kleindorfer S (2008) Genetic variation in the invasive avian parasite, Philornis downsi (Diptera, Muscidae) on the Galápagos archipelago. BMC Ecol. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Dutech C, Barrès B, Bridier J, Robin C, Milgroom MG, Ravigné V (2012) The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol Ecol 21:3931–3946. CrossRefPubMedGoogle Scholar
  26. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. CrossRefGoogle Scholar
  27. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130. CrossRefPubMedGoogle Scholar
  28. Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604. CrossRefPubMedGoogle Scholar
  29. Estoup A et al (2010) Combining genetic, historical and geographical data to reconstruct the dynamics of bioinvasions: application to the cane toad Bufo marinus. Mol Ecol Resour 10:886–901. CrossRefPubMedGoogle Scholar
  30. Estoup A, Ravigné V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47:51–72. CrossRefGoogle Scholar
  31. 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. CrossRefPubMedGoogle Scholar
  32. Everett RA (2000) Patterns and pathways of biological invasions. Trends Ecol Evol 15:177–178. CrossRefGoogle Scholar
  33. Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135. CrossRefPubMedGoogle Scholar
  34. Facon B, Pointier J-P, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367. CrossRefPubMedGoogle Scholar
  35. Facon B et al (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427. CrossRefPubMedGoogle Scholar
  36. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  37. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek RC (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Marine Biol Biotechnol 3:294–299PubMedGoogle Scholar
  38. Foucaud J et al (2009) Reproductive system, social organization, human disturbance and ecological dominance in native populations of the little fire ant, Wasmannia auropunctata. Mol Ecol 18:5059–5073. CrossRefPubMedGoogle Scholar
  39. Foucaud J et al (2010) Worldwide invasion by the little fire ant: routes of introduction and eco-evolutionary pathways. Evol Appl 3:363–374. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Fountain T, Duvaux L, Horsburgh G, Reinhardt K, Butlin RK (2014) Human-facilitated metapopulation dynamics in an emerging pest species, Cimex lectularius. Mol Ecol 23:1071–1084. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Fournier D, de Biseau J-C, Aron S (2009) Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala. Mol Ecol 18:186–199. CrossRefPubMedGoogle Scholar
  42. Fournier D, Tindo M, Kenne M, Mbenoun Masse PS, Van Bossche V, De Coninck E, Aron S (2012) Genetic structure, nestmate recognition and behaviour of two cryptic species of the invasive big-headed ant Pheidole megacephala. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385. CrossRefPubMedGoogle Scholar
  44. Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079. CrossRefPubMedGoogle Scholar
  45. Glancey BM, Nickerson JCE, Wojcik D, Trager J, Banks WA, Adams CT (1987) The increasing incidence of the polygynous form of the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae), in Florida. Fla Entomol 70:400–402. CrossRefGoogle Scholar
  46. Goodisman MAD, Sankovich KA, Kovacs JL (2007) Genetic and morphological variation over space and time in the invasive fire ant Solenopsis invicta. Biol Invasions 9:571–584. CrossRefGoogle Scholar
  47. Goodnight KF, Queller DC (2000) Relatedness 5.0.8, 5.0.8 edn. Goodnight Software, HoustonGoogle Scholar
  48. Gotzek D, Axen HJ, Suarez AV, Helms Cahan S, Shoemaker D (2015) Global invasion history of the tropical fire ant: a stowaway on the first global trade routes. Mol Ecol 24:374–388. CrossRefPubMedGoogle Scholar
  49. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  50. Guillemaud T, Beaumont MA, Ciosi M, Cornuet J-M, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99. CrossRefPubMedGoogle Scholar
  51. Guillemaud T, Ciosi M, Lombaert E, Estoup A (2011) Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. C R Biol 334:237–246. CrossRefPubMedGoogle Scholar
  52. Herrera HW (2011) CDF checklist of Galapagos ants. Charles Darwin Foundation. Accessed Jan 2016
  53. Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952. CrossRefPubMedGoogle Scholar
  54. Holway D, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233. CrossRefGoogle Scholar
  55. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information Mol Ecol. Resources 9:1322–1332. CrossRefGoogle Scholar
  56. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18. CrossRefGoogle Scholar
  57. Jackson M (1994) Galápagos: a natural history. University of Calgary Press, CalgaryGoogle Scholar
  58. 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. CrossRefPubMedGoogle Scholar
  59. Keller SR, Gilbert KJ, Fields PD, Taylor DR (2012) Bayesian inference of a complex invasion history revealed by nuclear and chloroplast genetic diversity in the colonizing plant, Silene latifolia. Mol Ecol 21:4721–4734. CrossRefPubMedGoogle Scholar
  60. Knight D, Bangs MJ (2007) Cutaneous allergic vasculitis due to Solenopsis geminata (Hymenoptera: Formicidae) envenomation in Indonesia. Southeast Asian J Trop Med Public Health 38:808–813PubMedGoogle Scholar
  61. 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. CrossRefPubMedGoogle Scholar
  62. Kricher JC (2006) Galápagos: a natural history. Princeton University Press, PrincetonGoogle Scholar
  63. Lach L, Hooper-Bui LM (2010) Consequences of ant invasions. In: Lach L, Parr C, Abbott K (eds) Ant ecology. Oxford University Press, Oxford, pp 261–286Google Scholar
  64. Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070. CrossRefGoogle Scholar
  65. Lander TA, Oddou-Muratorio S, Prouillet-Leplat H, Klein EK (2011) Reconstruction of a beech population bottleneck using archival demographic information and Bayesian analysis of genetic data. Mol Ecol 20:5182–5196. CrossRefPubMedGoogle Scholar
  66. Lau JA, terHorst CP (2015) Causes and consequences of failed adaptation to biological invasions: the role of ecological constraints. Mol Ecol 24:1987–1998. CrossRefPubMedGoogle Scholar
  67. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888. CrossRefPubMedGoogle Scholar
  68. Linsley EG, Usinger RL (1966) Insects of the Galápagos Islands. Proc Calif Acad Sci 33:113–196Google Scholar
  69. Lockwood J, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell Scientific Press, OxfordGoogle Scholar
  70. Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol Harlequin ladybird. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lombaert E et al (2011) Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Mol Ecol 20:4654–4670. CrossRefPubMedGoogle Scholar
  72. Lubin YD (1984) Changes in the native fauna of the Galápagos Islands following invasion by the little red fire ant, Wasmannia auropunctata. Biol J Linn Soc Lond 21:229–242. CrossRefGoogle Scholar
  73. 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.[0689:BICEGC]2.0.CO;2 CrossRefGoogle Scholar
  74. Maderspacher F (2011) The benefits of bottlenecks. Curr Biol 21:R171–R173. CrossRefPubMedGoogle Scholar
  75. McGlynn TP (1999) The worldwide transfer of ants: geographical distribution and ecological invasions. J Biogeogr 26:535–548. CrossRefGoogle Scholar
  76. McNew SM, Clayton DH (2018) Alien invasion: biology of Philornis flies highlighting Philornis downsi, an introduced parasite of Galápagos birds. Annu Rev Entomol 63:369–387. CrossRefPubMedGoogle Scholar
  77. Nafus DM, Schreiner IH (1988) Parental care in a tropical nymphalid butterfly Hypolimnas anomala. Anim Behav 36:1425–1431. CrossRefGoogle Scholar
  78. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  79. O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817. CrossRefGoogle Scholar
  80. Passera L (1994) Characteristics of tramp species. In: Williams DF (ed) Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, pp 23–43Google Scholar
  81. Perfecto I (1994) Foraging behavior as a determinant of asymmetric competitive interaction between two ant species in a tropical agroecosystem. Oecologia 98:184–192. CrossRefPubMedGoogle Scholar
  82. Perrings C, Mooney H, Williamson M (eds) (2010) Bioinvasions and globalization: ecology, economics, management, and policy. Oxford University Press, OxfordGoogle Scholar
  83. Plentovich S, Hebshi A, Conant S (2009) Detrimental effects of two widespread invasive ant species on weight and survival of colonial nesting seabirds in the Hawaiian Islands. Biol Invasions 11:289–298. CrossRefGoogle Scholar
  84. Plowes RM, Lebrun EG, Brown BV, Gilbert LE (2009) A review of Pseudacteon (Diptera: Phoridae) that parasitize ants of the Solenopsis geminata complex (Hymenoptera: Formicidae). Ann Entomol Soc Am 102:937–958. CrossRefGoogle Scholar
  85. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  86. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275. CrossRefPubMedGoogle Scholar
  87. Rabitsch W (2011) The hitchhiker’s guide to alien ant invasions. Biocontrol 56:551–572. CrossRefGoogle Scholar
  88. Richardson DM (2011) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley, OxfordGoogle Scholar
  89. Risch SJ, Carroll CR (1982) Effect of a keystone predaceous ant, Solenopsis geminata, on arthropods in a tropical agroecosystem. Ecology 63:1979–1983. CrossRefGoogle Scholar
  90. Rius M, Turon X, Ordóñez V, Pascual M (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Roque-Albelo L, Causton C (1999) El Niño and introduced insects in the Galápagos Islands: different dispersal strategies, similar effects. Notícias de Galápagos 60:30–36Google Scholar
  92. Roque-Albelo L, Causton CE, Mieles A (2000) The ants of Marchena island, twelve years after the introduction of the little fire ant, Wasmannia auropunctata. Notícias de Galápagos 61:17–20Google Scholar
  93. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. CrossRefGoogle Scholar
  94. Ross KG (1993) The breeding system of the fire ant Solenopsis invicta: effects on colony genetic structure. Am Nat 141:554–576. CrossRefPubMedGoogle Scholar
  95. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284. CrossRefPubMedGoogle Scholar
  96. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  97. Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371. CrossRefGoogle Scholar
  98. Sax DF, Gaines SD, Brown JH (2002) Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am Nat 160:766–783. CrossRefPubMedGoogle Scholar
  99. Seppä P (1994) Sociogenetic organization of the ants Myrmica ruginodis and Myrmica lobicornis: number, relatedness and longevity of reproducing individuals. J Evol Biol 7:71–95. CrossRefGoogle Scholar
  100. Simberloff D (2013) Invasive species: what everyone needs to know. Oxford University Press, OxfordGoogle Scholar
  101. Simberloff D, Rejmanek M (eds) (2011) Encyclopedia of biological invasions. University of California Press, BerkeleyGoogle Scholar
  102. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32. CrossRefGoogle Scholar
  103. Simberloff D et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. CrossRefPubMedGoogle Scholar
  104. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279. CrossRefPubMedGoogle Scholar
  105. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651. CrossRefPubMedGoogle Scholar
  106. Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360. CrossRefPubMedGoogle Scholar
  107. Suarez AV, Holway DA, Ward PS (2005) The role of opportunity in the unintentional introduction of nonnative ants. Proc Natl Acad Sci USA 102:17032–17035. CrossRefPubMedGoogle Scholar
  108. Taber SW (2000) Fire ants. Texas A&M University Press, College StationGoogle Scholar
  109. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Toral-Granda MV et al (2017) Alien species pathways to the Galapagos Islands, Ecuador. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  111. Tschinkel WR (2006) The fire ants. Harvard University Press, CambridgeGoogle Scholar
  112. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953. CrossRefPubMedGoogle Scholar
  113. Tye A, Snell HL, Peck SB, Adsersen H (2002) Outstanding terrestrial features of the Galapagos archipelago. In: Bensted-Smith R (ed) A biodiversity vision for the Galapagos islands: based on an international workshop of conservation biologists. Charles Darwin Foundation, WWF, Puerto Ayora, Ecuador, pp 12–23Google Scholar
  114. Valles SM, Porter SD (2003) Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Insectes Soc 50:199–200. CrossRefGoogle Scholar
  115. Van Oosterhout C, 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. CrossRefGoogle Scholar
  116. Vargo EL (1993) Colony reproductive structure in a polygyne population of Solenopsis geminata (Hymenoptera: Formicidae). Ann Entomol Soc Am 86:441–449. CrossRefGoogle Scholar
  117. Verdu P et al (2009) Origins and genetic diversity of Pygmy hunter-gatherers from Western Central Africa. Curr Biol 19:312–318. CrossRefPubMedGoogle Scholar
  118. Vitousek PM (1988) Diversity and biological invasions of oceanic islands. In: Wilson EO (ed) Biodiversity. National Academic Press, Washington, pp 181–189Google Scholar
  119. Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468Google Scholar
  120. von Aesch L, Cherix D (2005) Introduced ant species and mechanisms of competition on Floreana Island (Galapagos, Ecuador). Sociobiology 45:463–481Google Scholar
  121. Walsh SJ, Mena CF (2013) Science and conservation in the Galapagos Islands—frameworks and perspectives. Springer, New YorkCrossRefGoogle Scholar
  122. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513Google Scholar
  123. Wauters N, Dekoninck W, Herrera H, Fournier D (2014) Distribution, behavioral dominance and potential impacts on endemic fauna of the tropical fire ant Solenopsis geminata (Hymenoptera: Myrmicinae) in the Galápagos archipelago. Pan-Pac Entomol 90:205–220. CrossRefGoogle Scholar
  124. Wauters N, Dekoninck W, Hendrickx F, Herrera HW, Fournier D (2016) Habitat association and coexistence of endemic and introduced ant species in Galápagos Islands. Ecol Entomol 41:40–50. CrossRefGoogle Scholar
  125. Way MJ, Islam Z, Heong KL, Joshi RC (1998) Ants in tropical irrigated rice: distribution and abundance, especially of Solenopsis geminata (Hymenoptera: Formicidae). Bull Entomol Res 88:467–476. CrossRefGoogle Scholar
  126. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. CrossRefPubMedGoogle Scholar
  127. Wetterer JK (2011) Worldwide spread of the tropical fire ant, Solenopsis geminata (Hymenoptera: Formicidae). Myrmecol News 14:21–35Google Scholar
  128. Wheeler WM (1919) Expedition of the California Academy of Sciences to the Galapagos Islands, 1905–1906. XIV. The ants of the Galapagos Islands. Proc Calif Acad Sci 4:259–297Google Scholar
  129. Williams DF, Whelan P (1991) Polygynous colonies of Solenopsis geminata (Hymenoptera: Formicidae) in the Galapagos Islands. Fla Entomol 74:368–371CrossRefGoogle Scholar
  130. Williams DF, Wilson MH (1986) Control of the fire ants Ochetomyrmex auropunctata and Solenopsis geminata on the Galapagos Islands. Annual Report of the Charles Darwin Research StationGoogle Scholar
  131. Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). Am Entomol 49:144–163. CrossRefGoogle Scholar
  132. Yang C-C, Ascunce MS, Luo L-Z, Shao J-G, Shih C-J, Shoemaker D (2012) Propagule pressure and colony social organization are associated with the successful invasion and rapid range expansion of fire ants in China. Mol Ecol 21:817–833. CrossRefPubMedGoogle Scholar
  133. Zenger KR, Richardson BJ, Vachot-Griffin AM (2003) A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12:789–794. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Unit of Evolutionary Biology and EcologyUniversité libre de BruxellesBrusselsBelgium
  2. 2.Royal Belgian Institute of Natural SciencesBrusselsBelgium

Personalised recommendations