Abstract
Assessing genomic diversity and population structure of non-indigenous species is crucial to develop adequate management strategies. However, in species with scarce material for DNA extraction, applying genomic techniques can be a difficult task. Here we set a protocol for small DNA samples combining whole genome amplification (WGA) and genotyping-by-sequencing (GBS). This protocol was applied to the worldwide invasive colonial ascidian Didemnum vexillum using a single zooid per colony. WGA–GBS performance was tested using half zooids, providing empirical demonstration for genotyping reliability. We analysed 296 individuals from 12 localities worldwide including native and the main invaded areas. Polymorphic loci datasets generated by locality, area and globally, identified genetic differentiation at all levels. The two groups found in Japan, the native area, matched Cytochrome Oxidase I clades and were strongly differentiated at the genomic level suggesting reproductive isolation. Our genomic analyses confirmed that only one clade spread worldwide. We also detected some clones, always within the same locality. Genetic diversity was high in both the introduced and in the native area. Three independent colonisation events determined the global distribution of the species, although population pairwise comparisons within each introduced genetic cluster were significant. Human-mediated transportation seems to drive the distribution pattern of this species worldwide and regionally, as there is a lack of isolation by distance within introduced areas. Diverse and well differentiated populations point to a high expansion potential of this worrisome worldwide invader.
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References
Abbott CL, Ebert D, Tabata A, Therriault TW (2011) Twelve microsatellite markers in the invasive tunicate, Didemnum vexillum, isolated from low genome coverage 454 pyrosequencing reads. Conserv Genet Resour 3:79–81. https://doi.org/10.1007/s12686-010-9294-2
Adrion JR, Kousathanas A, Pascual M et al (2014) Drosophila suzukii: the genetic footprint of a recent, worldwide invasion. Mol Biol Evol 31:3148–3163. https://doi.org/10.1093/molbev/msu246
Airoldi L, Turon X, Perkol-Finkel S, Rius M (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib 21:755–768. https://doi.org/10.1111/ddi.12301
Aldred N, Clare AS (2014) Mini-review: impact and dynamics of surface fouling by solitary and compound ascidians. Biofouling 30:259–270. https://doi.org/10.1080/08927014.2013.866653
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519
Bax N, Williamson A, Aguero M et al (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323. https://doi.org/10.1016/S0308-597X(03)00041-1
Benestan L, Gosselin T, Perrier C et al (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315. https://doi.org/10.1111/mec.13245
Ben-Shlomo R (2017) Invasiveness, chimerism and genetic diversity. Mol Ecol 26:6502–6509. https://doi.org/10.1111/mec.14364
Bishop JDD, Wood CA, Lévêque L et al (2015) Repeated rapid assessment surveys reveal contrasting trends in occupancy of marinas by non-indigenous species on opposite sides of the western English Channel. Mar Pollut Bull 95:699–706. https://doi.org/10.1016/J.MARPOLBUL.2014.11.043
Blair C, Campbell CR, Yoder AD (2015) Assessing the utility of whole genome amplified DNA for next-generation molecular ecology. Mol Ecol Resour 15:1079–1090. https://doi.org/10.1111/1755-0998.12376
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 B Biol Sci 279:2377–2385. https://doi.org/10.1098/rspb.2011.2610
Bouchemousse S, Liautard-Haag C, Bierne N, Viard F (2016) Distinguishing contemporary hybridization from past introgression with postgenomic ancestry-informative SNPs in strongly differentiated Ciona species. Mol Ecol 25:5527–5542. https://doi.org/10.1111/mec.13854
Bullard SG, Lambert G, Carman MR et al (2007) The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. J Exp Mar Biol Ecol 342:99–108. https://doi.org/10.1016/j.jembe.2006.10.020
Calderón I, Ortega N, Duran S et al (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810. https://doi.org/10.1111/j.1365-294X.2007.03276.x
Carlton JT, Cohen AN (2003) Episodic global disperal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J Biogeogr 30:1809–1820
Carreras C, Ordóñez V, Zane L et al (2017) Population genomics of an endemic Mediterranean fish: differentiation by fine scale dispersal and adaptation. Sci Rep 7:43417. https://doi.org/10.1038/srep43417
Casso M, Navarro M, Ordóñez V et al (2018) Seasonal patterns of settlement and growth of introduced and native ascidians in bivalve cultures in the Ebro Delta (NE Iberian Peninsula). Reg Stud Mar Sci 23:12–22. https://doi.org/10.1016/j.rsma.2017.11.002
Chown SL, Hodgins KA, Griffin PC et al (2015) Biological invasions, climate change and genomics. Evol Appl 8:23–46. https://doi.org/10.1111/eva.12234
Clark MS, Tanguy A, Jollivet D et al (2010) Populations and pathways: genomic approaches to understanding population structure and environmental adaptation melody. In: Cock J, Tessmar-Raible K, Boyen C, Viard F (eds) Introduction to marine genomics, vol 1. Advances in marine genomics. Springer, Dordrecht, pp 73–118
Cohen CS, McCann L, Davis T et al (2011) Discovery and significance of the colonial tunicate Didemnum vexillum in Alaska. Aquat Invasion 6:263–271. https://doi.org/10.3391/ai.2011.6.3.03
Darling JA, Galil BS, Carvalho GR et al (2017) Recommendations for developing and applying genetic tools to assess and manage biological invasions in marine ecosystems. Mar Policy 85:54–64. https://doi.org/10.1016/j.marpol.2017.08.014
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083
Dean FB, Hosono S, Fang L et al (2002) Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci 99:5261–5266
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. https://doi.org/10.1016/S0169-5347(98)01554-7
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
El Nagar A, Huys R, Bishop JDD (2010) Widespread occurrence of the Southern Hemisphere ascidian Corella eumyota Traustedt, 1882 on the Atlantic coast of Iberia. Aquat Invasions 5:169–173. https://doi.org/10.3391/ai.2010.5.2.06
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Erwin PM, Pineda MC, Webster N et al (2014) Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians. ISME J 8:575–588. https://doi.org/10.1038/ismej.2013.188
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Evans JS, Erwin PM, Shenkar N, López-Legentil S (2017) Introduced ascidians harbor highly diverse and host-specific symbiotic microbial assemblages. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-11441-4
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fidler AE, Bacq-Labreuil A, Rachmilovitz E, Rinkevich B (2018) Efficient dispersal and substrate acquisition traits in a marine invasive species via transient chimerism and colony mobility. PeerJ 6:e5006. https://doi.org/10.7717/peerj.5006
Forsström T, Ahmad F, Vasemägi A (2017) Invasion genomics: genotyping-by-sequencing approach reveals regional genetic structure and signatures of temporal selection in an introduced mud crab. Mar Biol 164:186. https://doi.org/10.1007/s00227-017-3210-1
Gagnaire PA, Broquet T, Aurelle D et al (2015) Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evol Appl 8:769–786
Gagnaire PA, Lamy JB, Cornette F et al (2018) Analysis of genome-wide differentiation between native and introduced populations of the cupped oysters Crassostrea gigas and Crassostrea angulata. Genome Biol Evol 10:2518–2534. https://doi.org/10.1093/gbe/evy194
Galil BS, Boero F, Campbell ML et al (2015) ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biol Invasions 17:973–976. https://doi.org/10.1007/s10530-014-0778-y
Gittenberger A (2007) Recent population expansions of non-native ascidians in The Netherlands. J Exp Mar Biol Ecol 342:122–126. https://doi.org/10.1016/j.jembe.2006.10.022
Goudet J, Jombart T (2015) hierfstat: estimation and tests of hierarchical F-statistics. R Packag version 004-22
Griffith K, Mowat S, Holt RHF et al (2009) First records in Great Britain of the invasive colonial ascidian Didemnum vexillum Kott, 2002. Aquat Invasions 4:581–590. https://doi.org/10.3391/ai.2009.4.4.3
Grogan KE, McGinnis GJ, Sauther ML et al (2016) Next-generation genotyping of hypervariable loci in many individuals of a non-model species: technical and theoretical implications. BMC Genom 17:204. https://doi.org/10.1186/s12864-016-2503-y
Grünwald NJ, Everhart SE, Knaus BJ, Kamvar ZN (2017) Best practices for population genetic analyses. Phytopathology 107:1000–1010. https://doi.org/10.1094/PHYTO-12-16-0425-RVW
Han T, Chang C-W, Kwekel JC et al (2012) Characterization of whole genome amplified (WGA) DNA for use in genotyping assay development. BMC Genom 13:217. https://doi.org/10.1186/1471-2164-13-217
Hapke A, Thiele D (2016) GIbPSs: a toolkit for fast and accurate analyses of genotyping-by-sequencing data without a reference genome. Mol Ecol Resour 16:979–990. https://doi.org/10.1111/1755-0998.12510
Hawes NA, Tremblay LA, Pochon X et al (2018) Effects of temperature and salinity stress on DNA methylation in a highly invasive marine invertebrate, the colonial ascidian Didemnum vexillum. PeerJ 6:e5003. https://doi.org/10.7717/peerj.5003
Hess JE, Swalla BJ, Moran P (2009) New molecular markers to genetically differentiate populations of Didemnum vexillum (Kott, 2002)-an invasive ascidian species. Aquat Invasions 4:299–310. https://doi.org/10.3391/ai.2009.4.2.1
Hudson ME (2008) Sequencing breakthroughs for genomic ecology and evolutionary biology. Mol Ecol Resour 8:3–17. https://doi.org/10.1111/j.1471-8286.2007.02019.x
Hudson J, Viard F, Roby C, Rius M (2016) Anthropogenic transport of species across native ranges: unpredictable genetic and evolutionary consequences. Biol Lett 12:20160620. https://doi.org/10.1098/rsbl.2016.0620
Ivanov V, Lee KM, Mutanen M (2018) Mitonuclear discordance in wolf spiders: genomic evidence for species integrity and introgression. Mol Ecol 27:1681–1695. https://doi.org/10.1111/mec.14564
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jeffery NW, DiBacco C, Van Wyngaarden M et al (2017) RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic. Ecol Evol 7:2513–2524. https://doi.org/10.1002/ece3.2872
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281
Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet 6:208. https://doi.org/10.3389/fgene.2015.00208
Kaplan KA, Hart DR, Hopkins K et al (2018) Invasive tunicate restructures invertebrate community on fishing grounds and a large protected area on Georges Bank. Biol Invasions 20:87–103. https://doi.org/10.1007/s10530-017-1517-y
Keenan K, McGinnity P, Cross TF et al (2013) Diversity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210X.12067
Kott P (2002) A complex didemnid ascidian from Whangamata, New Zealand. J Mar Biol Assoc United Kingdom 82:625–628. https://doi.org/10.1017/S0025315402005970
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kürn U, Rendulic S, Tiozzo S, Lauzon RJ (2011) Asexual propagation and regeneration in colonial ascidians. Biol Bull 221:43–61
Lambert G (2001) A global overview of ascidian introductions and their possible impact on the endemic fauna. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 249–257
Lambert G (2009) Adventures of a sea squirt sleuth: unraveling the identity of Didemnum vexillum, a global ascidian invader. Aquat Invasions 4:5–28. https://doi.org/10.3391/ai.2009.4.1.2
Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161
Lin Y, Chen Y, Yi C et al (2017) Genetic signatures of natural selection in a model invasive ascidian. Sci Rep 7:44080. https://doi.org/10.1038/srep44080
López-Legentil S, Turon X, Schupp P (2006) Chemical and physical defenses against predators in Cystodytes (Ascidiacea). J Exp Mar Biol Ecol 332:27–36. https://doi.org/10.1016/J.JEMBE.2005.11.002
López-Legentil S, Legentil ML, Erwin PM, Turon X (2015) Harbor networks as introduction gateways: contrasting distribution patterns of native and introduced ascidians. Biol Invasions 17:1623–1638. https://doi.org/10.1007/s10530-014-0821-z
McGeoch MA, Butchart SHM, Spear D et al (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108. https://doi.org/10.1111/j.1472-4642.2009.00633.x
Mercer JM, Whitlatch RB, Osman RW (2009) Potential effects of the invasive colonial ascidian (Didemnum vexillum Kott, 2002) on pebble-cobble bottom habitats in Long Island Sound, USA. Aquat Invasions 4:133–142. https://doi.org/10.3391/ai.2009.4.1.14
Minchin D, Sides E (2006) Appearance of a cryptogenic tunicate, a Didemnum sp. fouling marina pontoons and leisure craft in Ireland. Aquat Invasions 1:143–147. https://doi.org/10.3391/ai.2006.1.3.8
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492. https://doi.org/10.1890/070064
Morris JA, Carman MR (2012) Fragment reattachment, reproductive status, and health indicators of the invasive colonial tunicate Didemnum vexillum with implications for dispersal. Biol Invasions 14:2133–2140. https://doi.org/10.1007/s10530-012-0219-8
Onyango MG, Aitken NC, Jack C et al (2016) Genotyping of whole genome amplified reduced representation libraries reveals a cryptic population of Culicoides brevitarsis in the Northern Territory, Australia. BMC Genom 17:769. https://doi.org/10.1186/s12864-016-3124-1
Ordóñez V, Pascual M, Fernández-Tejedor M et al (2015) Ongoing expansion of the worldwide invader Didemnum vexillum (Ascidiacea) in the Mediterranean Sea: high plasticity of its biological cycle promotes establishment in warm waters. Biol Invasions 17:2075–2085. https://doi.org/10.1007/s10530-015-0861-z
Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138. https://doi.org/10.1890/1540-9295(2004)002%5b0131:bbwaao%5d2.0.co;2
Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Pérez-Portela R, Arranz V, Rius M, Turon X (2013) Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Sci Rep 3:3197. https://doi.org/10.1038/srep03197
Pérez-Portela R, Bumford A, Coffman B et al (2018) Genetic homogeneity of the invasive lionfish across the Northwestern Atlantic and the Gulf of Mexico based on Single Nucleotide Polymorphisms. Sci Rep 8:5062. https://doi.org/10.1038/s41598-018-23339-w
Pinard R, De Winter A, Sarkis GJ et al (2006) Assessment of whole genome amplification-induced bias through high-throughput, massively parallel whole genome sequencing. BMC Genom 7:216. https://doi.org/10.1186/1471-2164-7-216
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. https://doi.org/10.1371/journal.pone.0025495
Pineda MC, López-Legentil S, Turon X (2013) Year-round reproduction in a seasonal sea: biological cycle of the introduced ascidian Styela plicata in the Western Mediterranean. Mar Biol 160:221–230. https://doi.org/10.1007/s00227-012-2082-7
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2018) A language and environment for statistical computing
Reinhardt JF, Gallagher KL, Stefaniak L et al (2012) Material properties of Didemnum vexillum and prediction of tendril fragmentation. Mar Biol 159:2875–2884. https://doi.org/10.1007/s00227-012-2048-9
Rinkevich B (2005) Natural chimerism in colonial urochordates. J Exp Mar Biol Ecol 322:93–109. https://doi.org/10.1016/j.jembe.2005.02.020
Rinkevich B, Fidler AE (2014) Initiating laboratory culturing of the invasive ascidian Didemnum vexillum. Manag Biol Invasions 5:55–62. https://doi.org/10.3391/mbi.2014.5.1.05
Rinkevich B, Weissman IL (1987) A long-term study on fused subclones in the ascidian Botryllus schlosseri: the resorption phenomenon (Protochordata: Tunicata). J Zool 213:717–733. https://doi.org/10.1111/j.1469-7998.1987.tb03736.x
Rius M, Pineda MC, Turon X (2009) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11:2181–2194. https://doi.org/10.1007/s10530-008-9375-2
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. https://doi.org/10.1371/journal.pone.0035815
Rius M, Turon X, Bernardi G et al (2015) Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biol Invasions 17:869–885. https://doi.org/10.1007/s10530-014-0792-0
Ryman N, Palm S, André C et al (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045. https://doi.org/10.1111/j.1365-294X.2006.02839.x
Segovia NI, Gallardo-Escárate C, Poulin E, Haye PA (2017) Lineage divergence, local adaptation across a biogeographic break and artificial transport, shape the genetic structure in the ascidian Pyura chilensis. Sci Rep 7:44559. https://doi.org/10.1038/srep44559
Shenkar N, Swalla BJ (2011) Global diversity of Ascidiacea. PLoS ONE 6:e20657. https://doi.org/10.1371/journal.pone.0020657
Smith KF, Stefaniak L, Saito Y et al (2012) Increased inter-colony fusion rates are associated with reduced COI haplotype diversity in an invasive colonial ascidian Didemnum vexillum. PLoS ONE 7:e30473. https://doi.org/10.1371/journal.pone.0030473
Stefaniak L (2017) Mechanisms for invasion success by Didemnum vexillum (Chordata: Ascidiacea): observations versus manipulations. Biol Invasions 19:1213–1225. https://doi.org/10.1007/s10530-016-1317-9
Stefaniak L, Whitlatch RB (2014) Life history attributes of a global invader: factors contributing to the invasion potential of Didemnum vexillum. Aquat Biol 21:221–229. https://doi.org/10.3354/ab00591
Stefaniak L, Lambert G, Gittenberger A et al (2009) Genetic conspecificity of the worldwide populations of Didemnum vexillum Kott, 2002. Aquat Invasions 4:29–44. https://doi.org/10.3391/ai.2009.4.1.3
Stefaniak L, Zhang H, Gittenberger A et al (2012) Determining the native region of the putatively invasive ascidian Didemnum vexillum Kott, 2002. J Exp Mar Biol Ecol 422–423:64–71. https://doi.org/10.1016/j.jembe.2012.04.012
Stoecker D (1980) Relationships between chemical defense and ecology in benthic ascidians. Mar Ecol Prog Ser 3:257–265
Tagliapietra D, Keppel E, Sigovini M, Lambert G (2012) First record of the colonial ascidian Didemnum vexillum Kott, 2002 in the Mediterranean: Lagoon of Venice (Italy). BioInvasions Rec 1:247–254. https://doi.org/10.3391/bir.2012.1.4.02
Tepolt CK (2015) Adaptation in marine invasion: a genetic perspective. Biol Invasions 17:887–903. https://doi.org/10.1007/s10530-014-0825-8
Tepolt CK, Palumbi SR (2015) Transcriptome sequencing reveals both neutral and adaptive genome dynamics in a marine invader. Mol Ecol 24:4145–4158. https://doi.org/10.1111/mec.13294
Torkamaneh D, Laroche J, Belzile F (2016) Genome-wide SNP calling from Genotyping by Sequencing (GBS) data: a comparison of seven pipelines and two sequencing technologies. PLoS ONE 11:e0161333. https://doi.org/10.1371/journal.pone.0161333
Tyrrell MC, Byers JE (2007) Do artificial substrates favor nonindigenous fouling species over native species? J Exp Mar Biol Ecol 342:54–60. https://doi.org/10.1016/J.JEMBE.2006.10.014
Valentine PC, Carman MR, Blackwood DS, Heffron EJ (2007) Ecological observations on the colonial ascidian Didemnum sp. in a New England tide pool habitat. J Exp Mar Biol Ecol 342:109–121. https://doi.org/10.1016/J.JEMBE.2006.10.021
Velandia-Huerto CA, Gittenberger A, Brown FD et al (2016) Automated detection of ncRNAs in the draft genome sequence of a colonial tunicate: the carpet sea squirt Didemnum vexillum. BMC Genom 17:691. https://doi.org/10.1186/s12864-016-2934-5
Viard F, Comtet T (2015) Applications of DNA-based methods for the study of biological invasions. In: Canning-Clode J (ed) Biological invasions in changing ecosystems: vectors, ecological impacts, management and predictions. De Gruyter Open, Berlin, pp 411–435
Viard F, David P, Darling JA (2016) Marine invasions enter the genomic era: three lessons from the past, and the way forward. Curr Zool 62:629–642. https://doi.org/10.1093/cz/zow053
Watts AM, Hopkins GA, Goldstien SJ (2019) Chimerism and population dieback alter genetic inference related to invasion pathways and connectivity of biofouling populations on artificial substrata. Ecol Evol 9(6):3089–3104. https://doi.org/10.1002/ece3.4817
White T, van der Ende J, Nichols TE (2019) Beyond Bonferroni revisited: concerns over inflated false positive research findings in the fields of conservation genetics, biology, and medicine. Conserv Genet. https://doi.org/10.1007/s10592-019-01178-0
Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New York
Wulff JL (1991) Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. J Exp Mar Biol Ecol 149:227–247
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. https://doi.org/10.1111/j.1365-294X.2010.04837.x
Zhan A, Briski E, Bock DG et al (2015) Ascidians as models for studying invasion success. Mar Biol 162:2449–2470
Zvyagintsev AY, Sanamyan KE, Turanov SV, Kartavtsev YF (2016) Colonial ascidian Didemnum vexillum Kott, 2002 is an alien species in Peter the Great Bay (Sea of Japan). Russ J Biol Invasions 7:237–246. https://doi.org/10.1134/S2075111716030140
Acknowledgements
We are deeply indebted to all people that contributed providing samples for this study: Gretchen Lambert, Ian Davidson, Mike Page, Judith Pederson, and Frédérique Viard. We specially thank Margarita Fernández, Carles Bori, Davide Tagliapietra, Marco Sigovini and Irene Guarneri for their help during sampling in Ebro Delta and Venice; Marc Rius for help while sampling in UK, and Gaku Kumano for assistance with the Aomori sampling. This research was funded by the projects CHALLENGEN and PopCOmics (CTM2013-48163 and CTM2017-88080, MCIU/AEI/FEDER/UE) from the Spanish Government. MC was funded by a predoctoral FPI contract of the Spanish Government. This is a contribution from the Consolidated Research Group “Benthic Biology and Ecology” SGR2017-1120 (Catalan Government).
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XT and MP designed research. MC and XT collected samples. MC performed laboratory work, ran the bioinformatics pipeline, and wrote the first draft of the manuscript. All authors contributed to analyses, discussed and interpreted results, and revised the manuscript.
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Raw reads from all individuals, including information of location of all samples, can be found at NCBI SRA Bioproject PRJNA555829. The genotypic data used in the analyses of global, clade A and clade B individuals is available in Appendices S9 to S11. All loci datasets will be available upon request to the authors.
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Casso, M., Turon, X. & Pascual, M. Single zooids, multiple loci: independent colonisations revealed by population genomics of a global invader. Biol Invasions 21, 3575–3592 (2019). https://doi.org/10.1007/s10530-019-02069-8
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DOI: https://doi.org/10.1007/s10530-019-02069-8