Marine Biology

, Volume 160, Issue 7, pp 1645–1660 | Cite as

Mixed but not admixed: a spatial analysis of genetic variation of an invasive ascidian on natural and artificial substrates

  • Víctor Ordóñez
  • Marta Pascual
  • Marc Rius
  • Xavier Turon
Original Paper

Abstract

Following the introduction to a new area (pre-border dispersal), post-border processes determine the success in the establishment of non-indigenous species (NIS). However, little is known on how these post-border processes shape the genetic composition of NIS at regional scales. Here, we analyse genetic variation in introduced populations along impacted coastlines to infer demographic and kinship dynamics at the post-border stage. We used as a model system the ascidian species Microcosmus squamiger that has been introduced worldwide. This species can colonize and grow fast on man-made artificial structures, impacting activities such as mariculture. However, it can also establish itself on natural substrates, thus altering natural communities and becoming an ecological problem. We genotyped 302 individuals from eight populations established on natural and artificial substrates in the north-western Mediterranean Sea, using six microsatellite loci. We then compared the resulting genotypes with those found within the native range of the species. We found high levels of genetic diversity and allelic richness in all populations, with an overall deficit of heterozygotes. Autocorrelation analyses showed that there was no within-population genetic structure (at a scale of tens of metres); likewise, no significant differentiation in pairwise comparisons between populations (tens of kilometres apart) and no isolation-by-distance pattern was found. The results suggest that M. squamiger has a natural capacity for high dispersal from one patch of hard substrate to another and no differences whatsoever could be substantiated between natural and artificial substrates. Interestingly, two groups of genetically differentiated individuals were detected that were associated with the two ancestral source areas of the worldwide expansion of the species. Individual assignment tests showed the coexistence of individuals of these two clusters in all populations but with little interbreeding among them as the frequency of admixed individuals was only 15 %. The mechanism responsible for maintaining these genetic pools unmixed is unknown, but it does not appear to compromise post-border colonization of introduced populations.

Supplementary material

227_2013_2217_MOESM1_ESM.docx (111 kb)
Supplementary material 1 (DOCX 112 kb)

References

  1. Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405Google Scholar
  2. Airoldi L, Bulleri F (2011) Anthropogenic disturbance can determine the magnitude of opportunistic species responses on marine urban infrastructures. PLoS One 6:e22985. doi:10.1371/journal.pone.0022985 CrossRefGoogle Scholar
  3. Bacchiocchi F, Airoldi L (2003) Distribution and dynamics of epibiota on hard structures for coastal protection. Estuar Coast Shelf Sci 56:1157–1166CrossRefGoogle Scholar
  4. Barros R, Rocha R, Pie M (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquat Invasions 4:45–57CrossRefGoogle Scholar
  5. Bax N, Carlton JT, Mathews-Amos A, Haedrich RL, Howarth FG, Purcell JE, Rieser A, Gray A (2001) The control of biological invasions in the world’s oceans. Conserv Biol 15:1234–1246CrossRefGoogle Scholar
  6. Belkhir K, Borsa P, Chikhi P, Raufaste N, Bonhomme F (2004) GENETIX 4.05.2, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier, FranceGoogle Scholar
  7. Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. TREE 26:333–339Google Scholar
  8. Blanquer A, Uriz M-J, Caujapé-Castells J (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Mar Ecol Prog Ser 380:95–102CrossRefGoogle Scholar
  9. Blum JC, Chang AL, Liljesthröm M, Schenk ME, Steinberg MK, Ruiz GM (2007) The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness. J Exp Mar Biol Ecol 342:5–14CrossRefGoogle Scholar
  10. Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytillus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215CrossRefGoogle Scholar
  11. Bulleri F, Airoldi L (2005) Artificial marine structures facilitate the spread of a non-indigenous green alga, Codium fragile ssp. tomentosoides, in the north Adriatic Sea. J Appl Ecol 42:1063–1072CrossRefGoogle Scholar
  12. Bulleri F, Chapman MG (2010) The introduction of coastal infrastructure as a driver of change in marine environments. J Appl Ecol 47:26–35CrossRefGoogle Scholar
  13. Calderón I, Ortega N, Durán S, Pascual M, Turon X (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810CrossRefGoogle Scholar
  14. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  15. Castilla JC, Manríquez PH, Delgado AP, Gargallo L, Leiva A, Radic D (2007) Bio-foam enhances larval retention in a free-spawning marine tunicate. Proc Natl Acad Sci USA 104:18120–18122CrossRefGoogle Scholar
  16. David GK, Marshall DJ, Riginos C (2010) Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata. Mar Biol 157:1955–1965CrossRefGoogle Scholar
  17. Dijkstra J, Harris LG, Westeman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68CrossRefGoogle Scholar
  18. Dumont CP, Gaymer CF, Thiel M (2011) Predation contributes to invasion resistance of benthic communities against the non-indigenous tunicate Ciona intestinalis. Biol Invasions 13:2023–2034CrossRefGoogle Scholar
  19. Dupont L, Viard F, Dowell MJ, Wood C, Bishop JDD (2009) Fine- and regional-scale genetic structure of the exotic ascidian Styela clava (Tunicata) in southwest England, 50 years after its introduction. Mol Ecol 18:442–453CrossRefGoogle Scholar
  20. Evanno C, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  21. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolut Bioinformatics Online 1:47–50Google Scholar
  22. Facon B, Pointier JP, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367CrossRefGoogle Scholar
  23. Fauvelot C, Bertozzi F, Costantini F, Airoldi L, Abbiati M (2009) Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats. Mar Biol 156:2313–2323CrossRefGoogle Scholar
  24. Fenster CB, Vekemans X, Hardy OJ (2003) Quantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae). Evolution 57:995–1007Google Scholar
  25. Forrest BM, Gardner JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54CrossRefGoogle Scholar
  26. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393CrossRefGoogle Scholar
  27. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G(ST) and D: forget G(ST) but not all of statistics! Mol Ecol 19:3845–3852CrossRefGoogle Scholar
  28. Glasby TM, Connell SD, Holloway MG, Hewitt CL (2007) Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar Biol 151:887–895CrossRefGoogle Scholar
  29. Gloor GB, Preston CR, Johnson-Schlitz DM, Nassif NA, Phillis RW, Benz WK, Robertson HM, Engels WR (1993) Type I repressors of P element mobility. Genetics 135:81–95Google Scholar
  30. Goldstien SJ, Schiel DR, Gemmell NJ (2010) Regional connectivity and coastal expansion: differentiating pre-border and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885CrossRefGoogle Scholar
  31. Goldstien SJ, Dupont L, Viard F, Hallas PJ, Nishikawa T et al (2011) Global Phylogeography of the Widely Introduced North West Pacific Ascidian Styela clava. PLoS One 6:e16755. doi:10.1371/journal.pone.0016755 CrossRefGoogle Scholar
  32. Goudet J (2002) FSTAT version 2.9.3.2. Available from Jerome.goudet @ie.zea.unil.ch, via email. Institute of Ecology, UNIL, CH-1015, Lausanne, SwitzerlandGoogle Scholar
  33. Grosberg R, Cunningham CW (2001) Genetic structure in the sea. From populations to communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Inc., Sunderland, pp 61–84Google Scholar
  34. Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation análisis and population genetics models. Heredity 83:145–154CrossRefGoogle Scholar
  35. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  36. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638Google Scholar
  37. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  38. Heywood JS (1991) Spatial analysis of genetic variation in plant populations. Annu Rev Ecol Syst 22:335–355CrossRefGoogle Scholar
  39. Howes S, Herbinger CM, Darnell P, Vercaemer B (2007) Spatial and temporal patterns of recruitment of the tunicate Ciona intestinalis on a mussel farm in Nova Scotia, Canada. J Exp Mar Biol Ecol 342:85–92CrossRefGoogle Scholar
  40. Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  41. Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847CrossRefGoogle Scholar
  42. 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 23:1801–1806CrossRefGoogle Scholar
  43. Jakobsson M, Edge MD, Rosenberg NA (2013) The relationship between F ST and the frequency of the most frequent allele. Genetics 193:515–528CrossRefGoogle Scholar
  44. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefGoogle Scholar
  45. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94 CrossRefGoogle Scholar
  46. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026CrossRefGoogle Scholar
  47. Jost L (2009) D vs. G ST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091CrossRefGoogle Scholar
  48. Kelly DW, Muirhead JR, Heath DD, MacIsaac HJ (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol Ecol 15:3641–3653CrossRefGoogle Scholar
  49. 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 4:434–437CrossRefGoogle Scholar
  50. Kott P (1985) The Australian Ascidiacea Pt 1, Phlebobranchia and Stolidobranchia. Mem Qld Mus 23:1–440Google Scholar
  51. Lacoursière-Roussel A, Bock DG, Cristescu ME, Guichard F, Girard P, Legendre P, McKindsey CW (2012) Disentangling invasion processes in a dynamic shipping-boating network. Mol Ecol 21:4227–4241CrossRefGoogle Scholar
  52. Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56:291–298CrossRefGoogle Scholar
  53. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4CrossRefGoogle Scholar
  54. Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688CrossRefGoogle Scholar
  55. Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161CrossRefGoogle Scholar
  56. Ledoux JB, Garrabou J, Bianchimani O, Drap P, Féral JP, Aurelle D (2010) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4202–4216Google Scholar
  57. Lejeusne C, Bock DG, Therriault TW, MacIsaac HJ, Cristescu ME (2011) Comparative phylogeography of two colonial ascidians reveals contrasting invasions histories in North America. Biol Invasions 13:635–650CrossRefGoogle Scholar
  58. Locke A (2009) A screening procedure for potential tunicate invaders of Atlantic Canada. Aquat Invasion 4:71–79CrossRefGoogle Scholar
  59. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  60. Lombaert E, Guillemaud T, Thomas CE, Lawson Handley LJ, Li J, Wang S, Pang H, Goryacheva I, Zakharov IA, Jousselin E, Poland RL, Migeon A, van Lenteren J, De Clercq P, Berkvens N, Jones W, Estoup A (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 20:4654–4670CrossRefGoogle Scholar
  61. López-Legentil S, Turon X, Planes S (2006) Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Mol Ecol 15:3957–3967CrossRefGoogle Scholar
  62. Marshall DJ (2002) In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate. Mar Ecol Prog Ser 236:113–119CrossRefGoogle Scholar
  63. McIvor L, Maggs CA, Provan J, Stanhope J (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919CrossRefGoogle Scholar
  64. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Res 11:5–18CrossRefGoogle Scholar
  65. Meusnier I, Valero M, Destombe C, Godé C, Desmarais E, Bonhomme F, Stam WT, Olsen JL (2002) Polymerase chain reaction-single strand conformation polymorphism analyses of nuclear and chloroplast DNA provide evidence for recombination, multiple introductions and nascent speciation in the Caulerpa taxifolia complex. Mol Ecol 11:2317–2325CrossRefGoogle Scholar
  66. Michaelsen VW (1927) Einige neue westaustralische ptychobranchiate Ascidien. Zool Anz 71:193–203Google Scholar
  67. Mokhtar-Jamaï K, Pascual M, Ledoux JB, Coma R, Féral JP, Garrabou J, Aurelle D (2011) From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Mol Ecol 20:3291–3305CrossRefGoogle Scholar
  68. Monniot C (1981) Apparition de l’ascidie Microcosmus exasperatus dans les ports Méditerranéens. Téthys 10:59–62Google Scholar
  69. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787CrossRefGoogle Scholar
  70. Osman RW, Whitlatch RB (2007) Variation in the ability of Didemnum sp. to invade established communities. J Exp Mar Biol Ecol 342:40–53CrossRefGoogle Scholar
  71. Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Ann Rev Environ Res 29:31–68CrossRefGoogle Scholar
  72. Park SDE (2001) Trypanotolerance in West African Cattle and the Population Genetic Effects of Selection [Ph.D. thesis] University of DublinGoogle Scholar
  73. Pérez-Portela R, Turon X, Bishop JDD (2012) Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Mar Ecol Prog Ser 451:93–105CrossRefGoogle Scholar
  74. Petersen JK, Svane I (1995) Larval dispersal in the ascidian Ciona intestinallis (L.). Evidence for a closed population. J Exp Mar Biol Ecol 186:89–102CrossRefGoogle Scholar
  75. Pineda MC, López-Legentil S, Turon X (2011) The whereabouts of an ancient wanderer: global phylogeography of the solitary ascidian Styela plicata. PLoS One 6:e25495. doi:10.1371/journal.pone.0025495 CrossRefGoogle Scholar
  76. Pinn EH, Mitchell K, Corkill J (2005) The assemblages of groynes in relation to substratum age, aspect and microhabitat. Estuar Coast Shelf Sci 62:271–282CrossRefGoogle Scholar
  77. Piry S, Alapetite A, Cournet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefGoogle Scholar
  78. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  79. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  80. Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185CrossRefGoogle Scholar
  81. Rius M, Pascual M, Turon X (2008a) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828CrossRefGoogle Scholar
  82. Rius M, Turon X, Pascual M (2008b) Isolation of polymorphic microsatellite loci for the marine invader Microcosmus squamiger (Ascidiacea). Mol Ecol Res 8:1405–1407CrossRefGoogle Scholar
  83. Rius M, Pineda MC, Turon X (2009) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11:2181–2194CrossRefGoogle Scholar
  84. Rius M, Turon X, Dias GM, Marshall DJ (2010) Propagule size effects across multiple life-history stages in a marine invertebrate. Funct Ecol 24:685–693CrossRefGoogle Scholar
  85. Rius M, Turon X, Ordóñez V, Pascual M (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS One 7:e35815. doi:10.1371/journal.pone.0035815 CrossRefGoogle Scholar
  86. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. TREE 22:454–464Google Scholar
  87. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  88. Rousset F (2000) Genetic differentiation between individuals. J Evolut Biol 13:58–62CrossRefGoogle Scholar
  89. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632Google Scholar
  90. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  91. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169CrossRefGoogle Scholar
  92. Simkanin C, Davidson IC, Dower JF, Jamieson G, Therriault TW (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499–511CrossRefGoogle Scholar
  93. Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowitz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Inc., Sunderland, pp 41–64Google Scholar
  94. Svane I, Havenhand JN (1993) Spawning and dispersal in Ciona intestinallis (L.). Mar Ecol 14:53–66CrossRefGoogle Scholar
  95. Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90Google Scholar
  96. Turon X, Nishikawa T, Rius M (2007) Spread of Microcosmus squamiger (Ascidiacea: Pyuridae) in the Mediterranean Sea and adjacent waters. J Exp Mar Biol Ecol 342:185–188CrossRefGoogle Scholar
  97. Tyrrell MC, Byers JE (2007) Do artificial substrates favor nonindigenous fouling species over native species? J Exp Mar Biol Ecol 342:54–60CrossRefGoogle Scholar
  98. Vaselli S, Bulleri F, Benedetti-Cecchi L (2008) Hard coastal-defence structures as habitats for native and exotic rocky-bottom species. Mar Environ Res 66:395–403CrossRefGoogle Scholar
  99. Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JS (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol Conserv 102:143–153CrossRefGoogle Scholar
  100. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  101. Whitlock MC (2011) G’ST and D do not replace FST. Mol Ecol 20:1083–1091CrossRefGoogle Scholar
  102. Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. TREE 24:136–144Google Scholar
  103. Wonham MJ, Walton WC, Ruiz GM, Frese AM, Galil BS (2001) Going to the source: role of the invasion pathway in determining potential invaders. Mar Ecol Prog Ser 215:1–12CrossRefGoogle Scholar
  104. Wotton DM, Hewitt CL (2004) Marine biosecurity post-border management: developing incursion response systems for New Zealand. N Z J Mar Fresh Res 38:553–559CrossRefGoogle Scholar
  105. Zhan A, MacIsaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694CrossRefGoogle Scholar
  106. Zhan A, Darling JA, Bock DG, Lacoursière-Roussel A, MacIsaac HJ, Cristescu ME (2012) Complex genetic patterns in closely related colonizing invasive species. Ecol Evol 2:1331–1346CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Víctor Ordóñez
    • 1
  • Marta Pascual
    • 1
  • Marc Rius
    • 2
    • 3
  • Xavier Turon
    • 3
  1. 1.Departament de Genètica, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Department of Evolution and EcologyUniversity of CaliforniaDavisUSA
  3. 3.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)BlanesSpain

Personalised recommendations