Biological Invasions

, Volume 17, Issue 3, pp 869–885 | Cite as

Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes

  • Marc Rius
  • Xavier Turon
  • Giacomo Bernardi
  • Filip A. M. Volckaert
  • Frédérique Viard
Molecular Tools

Abstract

Over the last 15 years studies on invasion genetics have provided important insights to unravel cryptic diversity, track the origin of colonizers and reveal pathways of introductions. Despite all these advances, to date little is known about how evolutionary processes influence the observed genetic patterns in marine biological invasions. Here, firstly we review the literature on invasion genetics that include samples from European seas. These seas constitute a wide array of unique water masses with diverse degrees of connectivity, and have a long history of species introductions. We found that only a small fraction of the recorded introduced species has been genetically analysed. Furthermore, most studies restrict their approach to describe patterns of cryptic diversity and genetic structure, with the underlying mechanisms involved in the invasion process being largely understudied. Secondly, we analyse how genetic, reproductive and anthropogenic traits shape genetic patterns of marine introduced species. We found that most studies reveal similar genetic diversity values in both native and introduced ranges, report evidence of multiple introductions, and show that genetic patterns in the introduced range are not explained by taxonomic group or reproductive strategy. Finally, we discuss the evolutionary implications derived from genetic patterns observed in non-indigenous species. We identify different scenarios that are determined by propagule pressure, phenotypic plasticity and pre-adaptation, and the effects of selection and genetic admixture. We conclude that there is a need for further investigations of evolutionary mechanisms that affect individual fitness and adaptation to rapid environmental change.

Keywords

Europe Hybridisation Introduced species Invasion routes Cryptic invasion Population genetics 

Supplementary material

10530_2014_792_MOESM1_ESM.pdf (72 kb)
Supplementary material 1 (PDF 73 kb)

References

  1. Acosta H, Forrest BM (2009) The spread of marine non-indigenous species via recreational boating: a conceptual model for risk assessment based on fault tree analysis. Ecol Model 220:1586–1598Google Scholar
  2. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709PubMedGoogle Scholar
  3. Angeloni F, Wagemaker N, Vergeer P et al (2012) Genomic toolboxes for conservation biologists. Evol Appl 5:130–143PubMedCentralPubMedGoogle Scholar
  4. Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202PubMedGoogle Scholar
  5. Audzijonyte A, Wittmann KJ, Väinölä R (2007) Tracing recent invasions of the Ponto-Caspian mysid shrimp Hemimysis anomala across Europe and to North America with mitochondrial DNA. Divers Distrib 14:179–186Google Scholar
  6. Audzijonyte A, Haugstetter J, Arbačiauskas K (2013) Characterization of ten polymorphic microsatellite markers in an invasive Ponto-Caspian mysid crustacean Paramysis lacustris. Conserv Genet Res 6:309–311Google Scholar
  7. Ayre DJ, Minchinton TE, Perrin C (2009) Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Mol Ecol 18:1887–1903PubMedGoogle Scholar
  8. Azzurro E, Golani D, Bucciarelli G et al (2006) Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. JEMBE 333:190–201Google Scholar
  9. Balanyà J, Segarra C, Prevosti A et al (1994) Colonization of America by Drosophila subobscura: the founder event and a rapid expansion. J Hered 85:427–432PubMedGoogle Scholar
  10. Barrett RD, Schluter D (2008) Adaptation from standing genetic variation. TREE 23:38–44PubMedGoogle Scholar
  11. Belmaker J, Parravicini V, Kulbicki M (2013) Ecological traits and environmental affinity explain Red Sea fish introduction into the Mediterranean. Glob Change Biol 19:1373–1382Google Scholar
  12. Bernardi G, Golani D, Azzurro E (2010) The genetics of Lessepsian bioinvasions. In: Golani D, Applebaum-Golani B (eds) Fish invasions of the Mediterranean Sea: change and renewal. Pensoft, Sofia, pp 71–84Google Scholar
  13. Bierne N, Welch J, Loire E et al (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072PubMedGoogle Scholar
  14. Blackburn TM, Pysek P, Bacher S et al (2011) A proposed unified framework for biological invasions. TREE 26:333–339PubMedGoogle Scholar
  15. Blank M, Bastrop R (2009) Phylogeny of the mud worm genus Marenzelleria (Polychaeta, Spionidae) inferred from mitochondrial DNA sequences. Zool Scri 38:313–321Google Scholar
  16. Blank M, Mikkat S, Verleih M et al (2012) Proteomic comparison of two invasive polychaete species and their naturally occurring F1-hybrids. J Prot Res 11:897–905Google Scholar
  17. Bock DG, Zhan A, Lejeusne C et al (2011) Looking at both sides of the invasion: patterns of colonization in the violet tunicate Botrylloides violaceus. Mol Ecol 20:503–516PubMedGoogle Scholar
  18. Bock DG, MacIsaac HJ, Cristescu ME (2012) Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian. Proc R Soc Biol Sci 279:2377–2385Google Scholar
  19. Bohmann K, Evans A, Gilbert MT et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. TREE 29:358–367PubMedGoogle Scholar
  20. Bolte S, Fuentes V, Haslob H et al (2013) Population genetics of the invasive ctenophore Mnemiopsis leidyi in Europe reveal source-sink dynamics and secondary dispersal to the Mediterranean Sea. MEPS 485:25–36Google Scholar
  21. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115PubMedGoogle Scholar
  22. Bott NJ, Ophel-Keller KM, Sierp MT et al (2010) Toward routine, DNA-based detection methods for marine pests. Biotechnol Adv 28:706–714PubMedGoogle Scholar
  23. Briski E, Bailey SA, Casas-Monroy O et al (2012) Relationship between propagule pressure and colonization pressure in invasion ecology: a test with ships’ ballast. Proc R Soc Biol Sci 279:2990–2997Google Scholar
  24. Brown JE, Stepien CA (2008) Ancient divisions, recent expansions: phylogeography and population genetics of the round goby Apollonia melanostoma. Mol Ecol 17:2598–2615PubMedGoogle Scholar
  25. Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA Barcoding of Marine Metazoa. Ann Rev Mar Sci 3:471–508PubMedGoogle Scholar
  26. Bulleri F, Airoldi L (2005) Artificial marine structures facilitate the spread of a nonindigenous green alga, Codium fragile ssp. tomentosoides, in the north Adriatic Sea. J Appl Ecol 42:1063–1072Google Scholar
  27. Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488Google Scholar
  28. Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? TREE 21:369–374PubMedGoogle Scholar
  29. Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106Google Scholar
  30. Carlton JT (2000) Quo vadimus exotica oceanica? Marine bioinvasion ecology in the twenty-first century. In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference. Massachusetts Institute of Technology Sea Grant College Program Cambridge, pp 6–23Google Scholar
  31. Carlton JT (2001) Introduced species in US coastal waters: environmental impacts and management priorities. Pew Oceans Commission, ArlingtonGoogle Scholar
  32. Carlton JT (2009) Deep Invasion Ecology and the Assembly of Communities in Historical Time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 13–56Google Scholar
  33. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82Google Scholar
  34. Ciosi M, Miller NJ, Toepfer S et al (2011) Stratified dispersal and increasing genetic variation during the invasion of Central Europe by the western corn rootworm, Diabrotica virgifera virgifera. Evol Appl 4:54–70PubMedCentralPubMedGoogle Scholar
  35. Clarke Murray C, Pakhomov EA, Therriault TW (2011) Recreational boating: a large unregulated vector transporting marine invasive species. Diversity Distrib 17:1161–1172Google Scholar
  36. Cock JM, Tessmar-Raible K, Boyen C et al (2010) Introduction to Marine Genomics. Springer, BerlinGoogle Scholar
  37. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558PubMedGoogle Scholar
  38. Coll M, Piroddi C, Steenbeck J et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE 5:e11842PubMedCentralPubMedGoogle Scholar
  39. Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886PubMedGoogle Scholar
  40. Cristescu MEA, Hebert PDN (2005) The “Crustacean Seas” - an evolutionary perspective on the Ponto Caspian peracarids. Can J Fish Aquat Sci 62:505–517Google Scholar
  41. Cristescu ME, Witt JD, Grigorovich IA et al (2004) Dispersal of the Ponto-Caspian amphipod Echinogammarus ischnus: invasion waves from the Pleistocene to the present. Heredity 92:197–203PubMedGoogle Scholar
  42. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329Google Scholar
  43. Dafforn KA, Johnston EL, Glasby TM (2009) Shallow moving structures promote marine invader dominance. Biofouling 25:277–287PubMedGoogle Scholar
  44. Daguin C, Borsa P (2000) Genetic relationships of Mytilus galloprovincialis Lamarck populations worldwide: evidence from nuclear-DNA markers. Geol Soc Lond 177:389–397Google Scholar
  45. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431PubMedGoogle Scholar
  46. Davies B, Villablanca FX, Roderick GK (1999) Bioinvasions of the medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153:351–360PubMedCentralPubMedGoogle Scholar
  47. Dawson MN, Hamner WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. PNAS 102:9235–9240PubMedCentralPubMedGoogle Scholar
  48. de Carvalho JF, Poulain J, Da Silva C et al (2013) Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Heredity 110:181–193Google Scholar
  49. Dijoux L, Viard F, Payri C (2014) The more we search, the more we find: discovery of a new lineage and a new species complex in the genus Asparagopsis. PLoS ONE 9:e103826  Google Scholar
  50. Dlugosch KM, Parker IM (2007) Molecular and quantitative trait variation across the native range of the invasive species Hypericum canariense: evidence for ancient patterns of colonization via pre-adaptation? Mol Ecol 16:4269–4283PubMedGoogle Scholar
  51. Drake JM (2006) Heterosis, the catapult effect and establishment success of a colonizing bird. Biol Lett 2:304–307PubMedCentralPubMedGoogle Scholar
  52. Dupont L, Ellien C, Viard F (2007a) Limits to gene flow in the slipper limpet Crepidula fornicata as revealed by microsatellite data and a larval dispersal model. MEPS 349:125–138Google Scholar
  53. Dupont L, Viard F, David P et al (2007b) Combined effects of bottlenecks and selfing in populations of Corella eumyota, a recently introduced sea squirt in the English Channel. Diversity Distrib 13:808–817Google Scholar
  54. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? PNAS 97:7043–7050PubMedCentralPubMedGoogle Scholar
  55. Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. TREE 23:619–630PubMedGoogle Scholar
  56. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130PubMedGoogle Scholar
  57. Everett MV, Grau ED, Seeb JE (2011) Short reads and nonmodel species: exploring the complexities of next-generation sequence assembly and SNP discovery in the absence of a reference genome. Mol Ecol Res 11:93–108Google Scholar
  58. Facon B, Genton BJ, Shykoff J et al (2006) A general eco-evolutionary framework for understanding bioinvasions. TREE 21:130–135PubMedGoogle Scholar
  59. Facon B, Pointier JP, Jarne P et al (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367PubMedGoogle Scholar
  60. Feldheim KA, Willink P, Brown JE et al (2009) Microsatellite loci for Ponto-Caspian gobies: markers for assessing exotic invasions. Mol Ecol Res 9:639–644Google Scholar
  61. Fierst JL (2011) A history of phenotypic plasticity accelerates adaptation to a new environment. J Evol Biol 24:1992–2001PubMedGoogle Scholar
  62. Forrest BM, Gardner JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54Google Scholar
  63. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385PubMedGoogle Scholar
  64. Fuller P, Benson A, Maynard E et al (2014) Neogobius melanostomus. USGS Nonindigenous Aquatic Species Database, GainesvilleGoogle Scholar
  65. Gaither MR, Toonen RJ, Bowen BW (2012) Coming out of the starting blocks: extended lag time rearranges genetic diversity in introduced marine fishes of Hawai’i. Proc R Soc Biol Sci 279:3948–3957Google Scholar
  66. Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bul 55:314–322Google Scholar
  67. Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean Sea. Biol Inv 11:359–372Google Scholar
  68. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Ann Rev Mar Sci 2:367–393PubMedGoogle Scholar
  69. Ghabooli S, Shiganova TA, Zhan A et al (2011) Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biol Invasions 13:679–690Google Scholar
  70. Ghabooli S, Shiganova TA, Briski E et al (2013) Invasion pathway of the ctenophore Mnemiopsis leidyi in the Mediterranean Sea. PLoS ONE 8:e81067PubMedCentralPubMedGoogle Scholar
  71. Glover KA, Pertoldi C, Besnier F et al (2013) Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs. BMC Genet 14:74PubMedCentralPubMedGoogle Scholar
  72. Golani D, Ritte U (1999) Genetic relationship in goatfishes (Mullidae: Perciformes) of the Red Sea and the Mediterranean, with remarks on Suez Canal migrants. Sci Mar 63:129–135Google Scholar
  73. Golani D, Azzuro E, Corsini-Foka M et al (2007) Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biol Lett 3:541–545PubMedCentralPubMedGoogle Scholar
  74. Goldstien SJ, Dupont L, Viard F et al (2011) Global phylogeography of the widely introduced north west Pacific ascidian Styela clava. PLoS ONE 6:e16755PubMedCentralPubMedGoogle Scholar
  75. Gollasch S (1996) Untersuchungen des Arteintrages durch den internationalen Schiffsverkehr unter besonderer Berücksichtigung nichtheimischer Arten. PhD, University of Hamburg, GermanyGoogle Scholar
  76. Gollasch S, Lenz J, Dammer M et al (2000) Survival of tropical ballast water organisms during a cruise from the Indian Ocean to the North Sea. J Plankton Res 22:923–937Google Scholar
  77. Gregg MC, Özsoy E (2002) Flow, water mass changes, and hydraulics in the Bosphorus. J Geophys Res 107:1–23Google Scholar
  78. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. TREE 17:22–27Google Scholar
  79. Grulois D, Leveque L, Viard F (2011) Mosaic genetic structure and sustainable establishment of the invasive kelp Undaria pinnatifida within a bay (Bay of St-Malo, Brittany). Cah Biol Mar 52:485–498Google Scholar
  80. Hansen MM, Olivieri I, Waller DM et al (2012) Monitoring adaptive genetic responses to environmental change. Mol Ecol 21:1311–1329PubMedGoogle Scholar
  81. Hassan M, Bonhomme F (2005) No reduction in neutral variability of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. J Fish Biol 66:865–870Google Scholar
  82. Hassan M, Harmelin-Vivien M, Bonhomme F (2003) Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus). JEMBE 291:219–232Google Scholar
  83. Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Divers Distrib 18:101–110Google Scholar
  84. Helyar SJ, Hemmer-Hansen J, Bekkevold D et al (2011) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Mol Ecol Res 11:123–136Google Scholar
  85. Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71Google Scholar
  86. Huey RB, Gilchrist GW, Hendry AP (2005) Using invasive species to study evolution: case studies with Drosophila and salmon. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates Inc., Sunderland, pp 139–164Google Scholar
  87. Kaluza P, Kölzsch A, Gastner MT et al (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103PubMedCentralPubMedGoogle Scholar
  88. Keller RP, Drake JM, Drew MB et al (2011) Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network. Divers Distrib 17:93–102Google Scholar
  89. Kochmann J, Carlsson J, Crowe TP et al (2012) Genetic evidence for the uncoupling of local aquaculture activities and a population of an invasive species - a case study of Pacific oysters (Crassostrea gigas). J Hered 103:661–671Google Scholar
  90. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. TREE 16:199–204PubMedGoogle Scholar
  91. Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591PubMedGoogle Scholar
  92. Koskinen MT, Sundell P, Piironen J et al (2002) Genetic assessment of spatiotemporal evolutionary relationships and stocking effects in grayling (Thymallus thymallus, Salmonidae). Ecol Lett 5:193–205Google Scholar
  93. Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446PubMedGoogle Scholar
  94. Lawson Handley LJ, Estoup A, Evans DM et al (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428Google Scholar
  95. Lee CE (2002) Evolutionary genetics of invasive species. TREE 17:386–391Google Scholar
  96. Lees DC, Lack HW, Rougerie R et al (2011) Tracking origins of invasive herbivores through herbaria and archival DNA: the case of the horse-chestnut leaf miner. Front Ecol Environ 9:322–328Google Scholar
  97. Lejeusne C, Chevaldonné P, Pergent-Martini C et al (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. TREE 25:250–260PubMedGoogle Scholar
  98. Leppäkoski E, Gollasch S, Gruszka P et al (2002) The Baltic - a sea of invaders. Can J Fish Aquat Sci 59:1175–1188Google Scholar
  99. Leung B, Drake JM, Lodge DM (2004) Predicting invasions: propagule pressure and the gravity of Allee effects. Ecology 85:1651–1660Google Scholar
  100. Meimberg H, Milan NF, Karatassiou M et al (2010) Patterns of introduction and adaptation during the invasion of Aegilops triuncialis (Poaceae) into Californian serpentine soils. Mol Ecol 19:5308–5319PubMedGoogle Scholar
  101. Menge BA, Chan F, Dudas S et al (2009) Do terrestrial ecologists ignore aquatic literature? Front Ecol Environ 7:182–183Google Scholar
  102. Mineur F, Belsher T, Johnson MP et al (2007) Experimental assessment of oyster transfers as a vector for macroalgal introductions. Biol Conserv 137:237–247Google Scholar
  103. Mineur F, Johnson MP, Maggs CA (2008) Macroalgal introductions by hull fouling on recreational vessels: seaweeds and sailors. Environ Manag 42:667–676Google Scholar
  104. Mineur F, Cook EJ, Minchin D et al (2012) Changing coasts: marine aliens and artificial structures. Oceanogr Mar Biol Ann Rev 50:189–234Google Scholar
  105. Murray JW, Top Z, Özsoy E (1991) Hydrographic properties and ventilation of the Black Sea. Deep Sea Res 38:S663–S689Google Scholar
  106. Neilson ME, Stepien CA (2011) Historic speciation and recent colonization of Eurasian monkey gobies (Neogobius fluviatilis and N. pallasi) revealed by DNA sequences, microsatellites, and morphology. Diversity Distrib 17:688–702Google Scholar
  107. Norkko J, Reed DC, Timmermann K et al (2012) A welcome can of worms? Hypoxia mitigation by an invasive species. Global Chang Biol 18:422–434Google Scholar
  108. Novak SJ (2007) The role of evolution in the invasion process. PNAS 104:3671–3672PubMedCentralPubMedGoogle Scholar
  109. Ordóñez V, Pascual M, Rius M et al (2013) Mixed but not admixed: a spatial analysis of genetic variation of an invasive ascidian on natural and artificial substrates. Mar Biol 160:1645–1660Google Scholar
  110. Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444PubMedGoogle Scholar
  111. Patti FP, Gambi MC (2001) Phylogeography of the invasive polychaete Sabella spallanzanii (Sabellidae) based on the nucleotide sequence of internal transcribed spacer 2 (ITS2) of nuclear rDNA. MEPS 215:169–177Google Scholar
  112. 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. MEPS 451:93–105Google Scholar
  113. Pérez-Portela R, Arranz V, Rius M et al (2013) Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Sci Rep 3:3197Google Scholar
  114. 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:e25495PubMedCentralPubMedGoogle Scholar
  115. Provan J, Murphy S, Maggs CA (2005) Tracking the invasive history of the green alga Codium fragile ssp. tomentosoides. Mol Ecol 14:189–194PubMedGoogle Scholar
  116. Reitzel AM, Herrera S, Layden MJ et al (2013) Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol Ecol 22:2953–2970PubMedCentralPubMedGoogle Scholar
  117. Reusch TB, Bolte S, Sparwel M et al (2010) Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world’s most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Mol Ecol 19:2690–2699PubMedGoogle Scholar
  118. Riquet F, Daguin-Thiebaut C, Ballenghien M et al (2013) Contrasting patterns of genome-wide polymorphism in the native and invasive range of the marine mollusc Crepidula fornicata. Mol Ecol 22:1003–1018PubMedGoogle Scholar
  119. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? TREE 29:233–242PubMedGoogle Scholar
  120. Rius M, Shenkar N (2012) Ascidian introductions through the Suez Canal: the case study of an Indo-Pacific species. Mar Pollut Bul 64:2060–2068Google Scholar
  121. Rius M, Teske PR (2013) Cryptic diversity in coastal Australasia: a morphological and mitonuclear genetic analysis of habitat-forming sibling species. Zool J Linn Soc 168:597–611Google Scholar
  122. Rius M, Turon X, Ordóñez V et al (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS ONE 7:e35815PubMedCentralPubMedGoogle Scholar
  123. Rius M, Clusella-Trullas S, McQuaid CD et al (2014) Range expansions across ecoregions: interactions of climate change, physiology and genetic diversity. Global Ecol Biogeogr 23:76–88Google Scholar
  124. Rohfritsch A, Bierne N, Boudry P et al (2013) Population genomics shed light on the demographic and adaptive histories of European invasion in the Pacific oyster, Crassostrea gigas. Evol Appl 6:1064–1078PubMedCentralPubMedGoogle Scholar
  125. Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc Biol Sci 273:2453–2459Google Scholar
  126. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. TREE 22:454–464PubMedGoogle Scholar
  127. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898PubMedGoogle Scholar
  128. Ruiz GM, Fofonoff PW, Carlton JT et al (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. AREES 31:481–531Google Scholar
  129. Sanna D, Merella P, Lai T et al (2011) Combined analysis of four mitochondrial regions allowed the detection of several matrilineal lineages of the lessepsian fish Fistularia commersonii in the Mediterranean Sea. J Mar Biol Ass UK 91:1289–1293Google Scholar
  130. Savini D, Occhipinti-Ambrogi A, Marchini A et al (2000) The top 27 animal alien species introduced into Europe for aquaculture and related activities. J Appl Ichthy 26:1–7Google Scholar
  131. Scammell GV (1981) The world encompassed: the first European maritime empires c. 800-1650. University of California PressGoogle Scholar
  132. Scammell GV (1991) The first imperial age: European overseas expansion 1500-1715. RoutledgeGoogle Scholar
  133. Seeb JE, Carvalho G, Hauser L et al (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Mol Ecol Res 11:1–8Google Scholar
  134. Seehausen O (2004) Hybridization and adaptive radiation. TREE 19:198–207PubMedGoogle Scholar
  135. Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385PubMedGoogle Scholar
  136. Siegel DA, Kinlan BP, Gaylord B et al (2003) Lagrangian descriptions of marine larval dispersion. MEPS 260:83–96Google Scholar
  137. Simon-Bouhet B, Garcia-Meunier P, Viard F (2006) Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France: evidence from mitochondrial sequence data. Mol Ecol 15:1699–1711PubMedGoogle Scholar
  138. Sorokin II (2002) The Black Sea: ecology and oceanography. BackhuysGoogle Scholar
  139. Stapley J, Reger J, Feulner PG et al (2010) Adaptation genomics: the next generation. TREE 25:705–712PubMedGoogle Scholar
  140. Strayer DL, Eviner VT, Jeschke JM et al (2006) Understanding the long-term effects of species invasions. TREE 21:645–651PubMedGoogle Scholar
  141. Streftaris N, Zenetos A (2006) Alien Marine Species in the Mediterranean - the 100 ‘worst invasives’ and their Impact. Mediterr Mar Sci 7:87–118Google Scholar
  142. Streftaris N, Zenetos A, Papathanassiou E (2005) Globalisation in marine ecosystems: the story of non-indigenous marine species across European Seas. Oceanogr Mar Biol Ann Rev 43:419–453Google Scholar
  143. Suarez AV, Holway DA, Ward PS (2005) The role of opportunity in the unintentional introduction of nonnative ants. PNAS 102:17032–17035PubMedCentralPubMedGoogle Scholar
  144. Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908Google Scholar
  145. Taylor DR, Keller SR (2007) Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61:334–345PubMedGoogle Scholar
  146. Tepolt CK, Darling JA, Bagley MJ et al (2009) European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population. Divers Distrib 15:997–1009Google Scholar
  147. Tsutsui ND, Suarez AV, Holway DA et al (2000) Reduced genetic variation and the success of an invasive species. PNAS 97:5948–5953PubMedCentralPubMedGoogle Scholar
  148. Turgeon J, Tayeh A, Facon B et al (2011) Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion. J Evol Biol 24:1044–1052PubMedGoogle Scholar
  149. Uriz MJ, Turon X (2012) Sponge ecology in the molecular era. Adv Mar Biol 61:345–410PubMedGoogle Scholar
  150. Vandepitte K, de Meyer T, Helsen K et al (2014) Rapid genetic adaptation precedes the spread of an exotic plant species. Mol Ecol 23:2157–2164PubMedGoogle Scholar
  151. Viard F, Ellien C, Dupont L (2006) Dispersal ability and invasion success of Crepidula fornicata in a single gulf: insights from genetic markers and larval-dispersal model. Helgol Mar Res 60:144–152Google Scholar
  152. Villablanca FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Mol Ecol 7:547–560PubMedGoogle Scholar
  153. Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. PNAS 102:5432–5437PubMedCentralPubMedGoogle Scholar
  154. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63PubMedCentralPubMedGoogle Scholar
  155. Wielgoss S, Taraschewski H, Meyer A et al (2008) Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Mol Ecol 17:3478–3495PubMedGoogle Scholar
  156. Wilson JRU, Dormontt EE, Prentis PJ et al (2009) Something in the way you move: dispersal pathways affect invasion. TREE 24:136–144PubMedGoogle Scholar
  157. Wolf JBW (2013) Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol Ecol Res 13:559–572Google Scholar
  158. Wolff WJ, Reise K (2002) Oyster imports as a vector for the introduction of alien species into northern and western european coastal waters. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 193–205Google Scholar
  159. Yaltırak C, Alpar B, Sakınç M et al (2000) Origin of the Strait of Çanakkale (Dardanelles): regional tectonics and the Mediterranean-Marmara incursion. Mar Geol 164:139–156Google Scholar
  160. Yap M, Man DL (1996) Colour, confusion and concessions: the history of the Chinese in South Africa. Hong Kong University Press, Hong KongGoogle Scholar
  161. Zenetos A, Gofas S, Morri C et al (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Mediterr Mar Sci 13:328–352Google Scholar
  162. Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694PubMedGoogle Scholar
  163. Zhan A, Darling JA, Bock DG et al (2012) Complex genetic patterns in closely related colonizing invasive species. Ecol Evol 2:1331–1346PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Marc Rius
    • 1
  • Xavier Turon
    • 2
  • Giacomo Bernardi
    • 3
  • Filip A. M. Volckaert
    • 4
  • Frédérique Viard
    • 5
    • 6
  1. 1.Ocean and Earth ScienceUniversity of Southampton, National Oceanography CentreSouthamptonUK
  2. 2.Centre for Advanced Studies of Blanes (CEAB-CSIC)BlanesSpain
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of California Santa CruzSanta CruzUSA
  4. 4.Laboratory of Biodiversity and Evolutionary Genomics, Department of BiologyUniversity of LeuvenLeuvenBelgium
  5. 5.Sorbonne Université, UPMC University Paris 06, Team Diversity and Connectivity in Coastal Marine Landscapes, UMR 7144, Station Biologique de RoscoffRoscoffFrance
  6. 6.CNRS, Laboratory Adaptation and Diversity in the Marine Environment, UMR 7144, Station Biologique de RoscoffRoscoffFrance

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