Skip to main content

Advertisement

SpringerLink
Log in

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

  • Molecular Tools
  • Published:
Biological Invasions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 220:1586–1598

    Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    CAS  PubMed  Google Scholar 

  • Angeloni F, Wagemaker N, Vergeer P et al (2012) Genomic toolboxes for conservation biologists. Evol Appl 5:130–143

    PubMed Central  CAS  PubMed  Google Scholar 

  • Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202

    CAS  PubMed  Google Scholar 

  • 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 14:179–186

    Google Scholar 

  • 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 6:309–311

    Google Scholar 

  • 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 18:1887–1903

    CAS  PubMed  Google Scholar 

  • Azzurro E, Golani D, Bucciarelli G et al (2006) Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. JEMBE 333:190–201

    Google Scholar 

  • Balanyà J, Segarra C, Prevosti A et al (1994) Colonization of America by Drosophila subobscura: the founder event and a rapid expansion. J Hered 85:427–432

    PubMed  Google Scholar 

  • Barrett RD, Schluter D (2008) Adaptation from standing genetic variation. TREE 23:38–44

    PubMed  Google Scholar 

  • Belmaker J, Parravicini V, Kulbicki M (2013) Ecological traits and environmental affinity explain Red Sea fish introduction into the Mediterranean. Glob Change Biol 19:1373–1382

    Google Scholar 

  • 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 71–84

    Google Scholar 

  • Bierne N, Welch J, Loire E et al (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072

    PubMed  Google Scholar 

  • Blackburn TM, Pysek P, Bacher S et al (2011) A proposed unified framework for biological invasions. TREE 26:333–339

    PubMed  Google Scholar 

  • Blank M, Bastrop R (2009) Phylogeny of the mud worm genus Marenzelleria (Polychaeta, Spionidae) inferred from mitochondrial DNA sequences. Zool Scri 38:313–321

    Google Scholar 

  • 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 11:897–905

    CAS  Google Scholar 

  • 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 20:503–516

    CAS  PubMed  Google Scholar 

  • 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 279:2377–2385

    Google Scholar 

  • Bohmann K, Evans A, Gilbert MT et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. TREE 29:358–367

    PubMed  Google Scholar 

  • 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 485:25–36

    Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115

    PubMed  Google Scholar 

  • Bott NJ, Ophel-Keller KM, Sierp MT et al (2010) Toward routine, DNA-based detection methods for marine pests. Biotechnol Adv 28:706–714

    CAS  PubMed  Google Scholar 

  • 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 279:2990–2997

    Google Scholar 

  • Brown JE, Stepien CA (2008) Ancient divisions, recent expansions: phylogeography and population genetics of the round goby Apollonia melanostoma. Mol Ecol 17:2598–2615

    CAS  PubMed  Google Scholar 

  • Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA Barcoding of Marine Metazoa. Ann Rev Mar Sci 3:471–508

    PubMed  Google Scholar 

  • 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 42:1063–1072

    Google Scholar 

  • Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488

    Google Scholar 

  • Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? TREE 21:369–374

    PubMed  Google Scholar 

  • Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Google Scholar 

  • 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 6–23

  • Carlton JT (2001) Introduced species in US coastal waters: environmental impacts and management priorities. Pew Oceans Commission, Arlington

    Google Scholar 

  • 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 13–56

    Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Google Scholar 

  • 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 4:54–70

    PubMed Central  CAS  PubMed  Google Scholar 

  • Clarke Murray C, Pakhomov EA, Therriault TW (2011) Recreational boating: a large unregulated vector transporting marine invasive species. Diversity Distrib 17:1161–1172

    Google Scholar 

  • Cock JM, Tessmar-Raible K, Boyen C et al (2010) Introduction to Marine Genomics. Springer, Berlin

    Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    CAS  PubMed  Google Scholar 

  • Coll M, Piroddi C, Steenbeck J et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE 5:e11842

    PubMed Central  PubMed  Google Scholar 

  • Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886

    CAS  PubMed  Google Scholar 

  • Cristescu MEA, Hebert PDN (2005) The “Crustacean Seas” - an evolutionary perspective on the Ponto Caspian peracarids. Can J Fish Aquat Sci 62:505–517

  • 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 92:197–203

    CAS  PubMed  Google Scholar 

  • Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329

    Google Scholar 

  • Dafforn KA, Johnston EL, Glasby TM (2009) Shallow moving structures promote marine invader dominance. Biofouling 25:277–287

    CAS  PubMed  Google Scholar 

  • Daguin C, Borsa P (2000) Genetic relationships of Mytilus galloprovincialis Lamarck populations worldwide: evidence from nuclear-DNA markers. Geol Soc Lond 177:389–397

    Google Scholar 

  • 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 14:419–431

    PubMed  Google Scholar 

  • Davies B, Villablanca FX, Roderick GK (1999) Bioinvasions of the medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153:351–360

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dawson MN, Hamner WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. PNAS 102:9235–9240

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 110:181–193

    Google Scholar 

  • 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  

  • 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 16:4269–4283

    CAS  PubMed  Google Scholar 

  • Drake JM (2006) Heterosis, the catapult effect and establishment success of a colonizing bird. Biol Lett 2:304–307

    PubMed Central  PubMed  Google Scholar 

  • 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 349:125–138

    Google Scholar 

  • 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 13:808–817

    Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? PNAS 97:7043–7050

    PubMed Central  CAS  PubMed  Google Scholar 

  • Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. TREE 23:619–630

    PubMed  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130

    PubMed  Google Scholar 

  • 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 11:93–108

    Google Scholar 

  • Facon B, Genton BJ, Shykoff J et al (2006) A general eco-evolutionary framework for understanding bioinvasions. TREE 21:130–135

    PubMed  Google Scholar 

  • 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 18:363–367

    CAS  PubMed  Google Scholar 

  • Feldheim KA, Willink P, Brown JE et al (2009) Microsatellite loci for Ponto-Caspian gobies: markers for assessing exotic invasions. Mol Ecol Res 9:639–644

    Google Scholar 

  • Fierst JL (2011) A history of phenotypic plasticity accelerates adaptation to a new environment. J Evol Biol 24:1992–2001

    CAS  PubMed  Google Scholar 

  • Forrest BM, Gardner JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54

    Google Scholar 

  • Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385

    CAS  PubMed  Google Scholar 

  • Fuller P, Benson A, Maynard E et al (2014) Neogobius melanostomus. USGS Nonindigenous Aquatic Species Database, Gainesville

  • 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 279:3948–3957

    Google Scholar 

  • Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bul 55:314–322

    CAS  Google Scholar 

  • Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean Sea. Biol Inv 11:359–372

    Google Scholar 

  • Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Ann Rev Mar Sci 2:367–393

    PubMed  Google Scholar 

  • Ghabooli S, Shiganova TA, Zhan A et al (2011) Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biol Invasions 13:679–690

    Google Scholar 

  • Ghabooli S, Shiganova TA, Briski E et al (2013) Invasion pathway of the ctenophore Mnemiopsis leidyi in the Mediterranean Sea. PLoS ONE 8:e81067

    PubMed Central  PubMed  Google Scholar 

  • 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 14:74

    PubMed Central  PubMed  Google Scholar 

  • 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 63:129–135

    Google Scholar 

  • 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 3:541–545

    PubMed Central  PubMed  Google Scholar 

  • Goldstien SJ, Dupont L, Viard F et al (2011) Global phylogeography of the widely introduced north west Pacific ascidian Styela clava. PLoS ONE 6:e16755

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gollasch S (1996) Untersuchungen des Arteintrages durch den internationalen Schiffsverkehr unter besonderer Berücksichtigung nichtheimischer Arten. PhD, University of Hamburg, Germany

  • 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 22:923–937

    Google Scholar 

  • Gregg MC, Özsoy E (2002) Flow, water mass changes, and hydraulics in the Bosphorus. J Geophys Res 107:1–23

    Google Scholar 

  • Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. TREE 17:22–27

    Google Scholar 

  • 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 52:485–498

    Google Scholar 

  • Hansen MM, Olivieri I, Waller DM et al (2012) Monitoring adaptive genetic responses to environmental change. Mol Ecol 21:1311–1329

    PubMed  Google Scholar 

  • Hassan M, Bonhomme F (2005) No reduction in neutral variability of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. J Fish Biol 66:865–870

    Google Scholar 

  • Hassan M, Harmelin-Vivien M, Bonhomme F (2003) Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus). JEMBE 291:219–232

    Google Scholar 

  • Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Divers Distrib 18:101–110

    Google Scholar 

  • 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 11:123–136

    Google Scholar 

  • Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71

    CAS  Google Scholar 

  • 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 139–164

    Google Scholar 

  • Kaluza P, Kölzsch A, Gastner MT et al (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103

    PubMed Central  PubMed  Google Scholar 

  • 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 17:93–102

    Google Scholar 

  • 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 103:661–671

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. TREE 16:199–204

    PubMed  Google Scholar 

  • Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591

    CAS  PubMed  Google Scholar 

  • 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 5:193–205

    Google Scholar 

  • Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446

    PubMed  Google Scholar 

  • Lawson Handley LJ, Estoup A, Evans DM et al (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428

    Google Scholar 

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

    Google Scholar 

  • 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 9:322–328

    Google Scholar 

  • 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 25:250–260

    PubMed  Google Scholar 

  • Leppäkoski E, Gollasch S, Gruszka P et al (2002) The Baltic - a sea of invaders. Can J Fish Aquat Sci 59:1175–1188

    Google Scholar 

  • Leung B, Drake JM, Lodge DM (2004) Predicting invasions: propagule pressure and the gravity of Allee effects. Ecology 85:1651–1660

    Google Scholar 

  • 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 19:5308–5319

    PubMed  Google Scholar 

  • Menge BA, Chan F, Dudas S et al (2009) Do terrestrial ecologists ignore aquatic literature? Front Ecol Environ 7:182–183

    Google Scholar 

  • Mineur F, Belsher T, Johnson MP et al (2007) Experimental assessment of oyster transfers as a vector for macroalgal introductions. Biol Conserv 137:237–247

    Google Scholar 

  • Mineur F, Johnson MP, Maggs CA (2008) Macroalgal introductions by hull fouling on recreational vessels: seaweeds and sailors. Environ Manag 42:667–676

    Google Scholar 

  • Mineur F, Cook EJ, Minchin D et al (2012) Changing coasts: marine aliens and artificial structures. Oceanogr Mar Biol Ann Rev 50:189–234

    Google Scholar 

  • Murray JW, Top Z, Özsoy E (1991) Hydrographic properties and ventilation of the Black Sea. Deep Sea Res 38:S663–S689

    Google Scholar 

  • 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 17:688–702

    Google Scholar 

  • Norkko J, Reed DC, Timmermann K et al (2012) A welcome can of worms? Hypoxia mitigation by an invasive species. Global Chang Biol 18:422–434

    Google Scholar 

  • Novak SJ (2007) The role of evolution in the invasion process. PNAS 104:3671–3672

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 160:1645–1660

    Google Scholar 

  • Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444

    PubMed  Google Scholar 

  • 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 215:169–177

    CAS  Google Scholar 

  • 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 451:93–105

    Google Scholar 

  • 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 3:3197

    Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Provan J, Murphy S, Maggs CA (2005) Tracking the invasive history of the green alga Codium fragile ssp. tomentosoides. Mol Ecol 14:189–194

    PubMed  Google Scholar 

  • 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 22:2953–2970

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 19:2690–2699

    CAS  PubMed  Google Scholar 

  • 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 22:1003–1018

    CAS  PubMed  Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? TREE 29:233–242

    PubMed  Google Scholar 

  • Rius M, Shenkar N (2012) Ascidian introductions through the Suez Canal: the case study of an Indo-Pacific species. Mar Pollut Bul 64:2060–2068

    CAS  Google Scholar 

  • 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 168:597–611

    Google Scholar 

  • Rius M, Turon X, Ordóñez V et al (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS ONE 7:e35815

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 23:76–88

    Google Scholar 

  • 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 6:1064–1078

    PubMed Central  PubMed  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc Biol Sci 273:2453–2459

    Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. TREE 22:454–464

    PubMed  Google Scholar 

  • Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898

    CAS  PubMed  Google Scholar 

  • Ruiz GM, Fofonoff PW, Carlton JT et al (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. AREES 31:481–531

    Google Scholar 

  • 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 91:1289–1293

    Google Scholar 

  • 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 26:1–7

    Google Scholar 

  • Scammell GV (1981) The world encompassed: the first European maritime empires c. 800-1650. University of California Press

  • Scammell GV (1991) The first imperial age: European overseas expansion 1500-1715. Routledge

  • 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 11:1–8

    Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. TREE 19:198–207

    PubMed  Google Scholar 

  • Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385

    PubMed  Google Scholar 

  • Siegel DA, Kinlan BP, Gaylord B et al (2003) Lagrangian descriptions of marine larval dispersion. MEPS 260:83–96

    Google Scholar 

  • 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 15:1699–1711

    CAS  PubMed  Google Scholar 

  • Sorokin II (2002) The Black Sea: ecology and oceanography. Backhuys

  • Stapley J, Reger J, Feulner PG et al (2010) Adaptation genomics: the next generation. TREE 25:705–712

    PubMed  Google Scholar 

  • Strayer DL, Eviner VT, Jeschke JM et al (2006) Understanding the long-term effects of species invasions. TREE 21:645–651

    PubMed  Google Scholar 

  • Streftaris N, Zenetos A (2006) Alien Marine Species in the Mediterranean - the 100 ‘worst invasives’ and their Impact. Mediterr Mar Sci 7:87–118

  • 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 43:419–453

    Google Scholar 

  • Suarez AV, Holway DA, Ward PS (2005) The role of opportunity in the unintentional introduction of nonnative ants. PNAS 102:17032–17035

    PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908

    Google Scholar 

  • Taylor DR, Keller SR (2007) Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61:334–345

    PubMed  Google Scholar 

  • 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 15:997–1009

    Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA et al (2000) Reduced genetic variation and the success of an invasive species. PNAS 97:5948–5953

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 24:1044–1052

    CAS  PubMed  Google Scholar 

  • Uriz MJ, Turon X (2012) Sponge ecology in the molecular era. Adv Mar Biol 61:345–410

    PubMed  Google Scholar 

  • Vandepitte K, de Meyer T, Helsen K et al (2014) Rapid genetic adaptation precedes the spread of an exotic plant species. Mol Ecol 23:2157–2164

    PubMed  Google Scholar 

  • 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 60:144–152

    Google Scholar 

  • Villablanca FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Mol Ecol 7:547–560

    CAS  PubMed  Google Scholar 

  • 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 102:5432–5437

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 17:3478–3495

    CAS  PubMed  Google Scholar 

  • Wilson JRU, Dormontt EE, Prentis PJ et al (2009) Something in the way you move: dispersal pathways affect invasion. TREE 24:136–144

    PubMed  Google Scholar 

  • Wolf JBW (2013) Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol Ecol Res 13:559–572

    CAS  Google Scholar 

  • 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 193–205

  • 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 164:139–156

  • Yap M, Man DL (1996) Colour, confusion and concessions: the history of the Chinese in South Africa. Hong Kong University Press, Hong Kong

  • 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 13:328–352

    Google Scholar 

  • Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694

    CAS  PubMed  Google Scholar 

  • Zhan A, Darling JA, Bock DG et al (2012) Complex genetic patterns in closely related colonizing invasive species. Ecol Evol 2:1331–1346

    PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Benoit Simon-Bouhet and Florentine Riquet for providing data and assistance in the design of some figures. We are grateful to the reviewers who provided comments that greatly improved the manuscript. Funding was provided by the European Union FP7 project COCONET (7th PM, Grant agreement #287844) and a number of other sources. F.Vi. acknowledges the HiFlo (ANR-08-BLAN-0334) and HySea (ANR-12-BSV7-0011) ANR programmes. X.T. is grateful to the Spanish Ministry of Science projects CTM2010-22218 and CTM2013-48163. The publication of this paper was supported by CONISMA, the Italian National Interuniversity Consortium for Marine Sciences, which received funding from the European Community’s Seventh Framework Programme (FP7/2007- 2013) for the project VECTORS (Vectors of Change in Oceans and Seas Marine Life, Impact on Economic Sectors, Grant agreement #266445, http://www.marine-vectors.eu). This paper stems from the International workshop MOLTOOLS (Molecular Tools for Monitoring Marine Invasive Species), held in Lecce, Italy, in September 2012. We thank Stefano Piraino and the project VECTORS for the invitation to this workshop.

Author information

Authors and Affiliations

  1. Ocean and Earth Science, University of Southampton, National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK

    Marc Rius

  2. Centre for Advanced Studies of Blanes (CEAB-CSIC), Accés Cala S Francesc 14, 17300, Blanes, Girona, Spain

    Xavier Turon

  3. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA, 95060, USA

    Giacomo Bernardi

  4. Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Charles Deberiotstraat 32, Box 2439, 3000, Leuven, Belgium

    Filip A. M. Volckaert

  5. Sorbonne Université, UPMC University Paris 06, Team Diversity and Connectivity in Coastal Marine Landscapes, UMR 7144, Station Biologique de Roscoff, 29680, Roscoff, France

    Frédérique Viard

  6. CNRS, Laboratory Adaptation and Diversity in the Marine Environment, UMR 7144, Station Biologique de Roscoff, 29680, Roscoff, France

    Frédérique Viard

Authors
  1. Marc Rius
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xavier Turon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giacomo Bernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Filip A. M. Volckaert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Frédérique Viard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc Rius.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 73 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rius, M., Turon, X., Bernardi, G. et al. Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biol Invasions 17, 869–885 (2015). https://doi.org/10.1007/s10530-014-0792-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0792-0

Keywords

Search

Navigation