Single zooids, multiple loci: independent colonisations revealed by population genomics of a global invader

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.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 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

    Article  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. Ben-Shlomo R (2017) Invasiveness, chimerism and genetic diversity. Mol Ecol 26:6502–6509. https://doi.org/10.1111/mec.14364

    CAS  Article  PubMed  Google Scholar 

  10. 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

    CAS  Article  PubMed  Google Scholar 

  11. 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

    CAS  Article  PubMed  Google Scholar 

  12. 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

    Article  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083

    Article  PubMed  Google Scholar 

  24. Dean FB, Hosono S, Fang L et al (2002) Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci 99:5261–5266

    CAS  Article  Google Scholar 

  25. Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  26. 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

    CAS  Article  PubMed  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 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

    CAS  Article  PubMed  Google Scholar 

  31. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    CAS  Article  Google Scholar 

  32. 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

    CAS  Article  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 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

    CAS  Article  Google Scholar 

  36. 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

    Article  Google Scholar 

  37. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. Goudet J, Jombart T (2015) hierfstat: estimation and tests of hierarchical F-statistics. R Packag version 004-22

  41. 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

    Article  Google Scholar 

  42. 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

    CAS  Article  Google Scholar 

  43. 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

    Article  PubMed  Google Scholar 

  44. 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

    CAS  Article  Google Scholar 

  45. 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

    CAS  Article  PubMed  Google Scholar 

  46. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 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

    Article  Google Scholar 

  48. 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

    CAS  Article  PubMed  Google Scholar 

  49. 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

    Article  PubMed  PubMed Central  Google Scholar 

  50. 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

    CAS  Article  PubMed  Google Scholar 

  51. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 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

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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

    CAS  Article  PubMed  Google Scholar 

  54. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  PubMed  PubMed Central  Google Scholar 

  56. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. 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

    Article  Google Scholar 

  58. 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

    Article  Google Scholar 

  59. 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

    Article  Google Scholar 

  60. 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

    CAS  Article  Google Scholar 

  61. Kürn U, Rendulic S, Tiozzo S, Lauzon RJ (2011) Asexual propagation and regeneration in colonial ascidians. Biol Bull 221:43–61

    Article  Google Scholar 

  62. 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

    Google Scholar 

  63. 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

    Article  Google Scholar 

  64. 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

    Article  Google Scholar 

  65. 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

    Article  PubMed  PubMed Central  Google Scholar 

  66. 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

    Article  Google Scholar 

  67. 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

    Article  PubMed  Google Scholar 

  68. 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

    Article  Google Scholar 

  69. 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

    Article  Google Scholar 

  70. 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

    Article  Google Scholar 

  71. 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

    Article  Google Scholar 

  72. 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

    Article  Google Scholar 

  73. 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

    CAS  Article  Google Scholar 

  74. 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

    Article  PubMed  PubMed Central  Google Scholar 

  75. 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

    Article  Google Scholar 

  76. 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

    CAS  Article  PubMed  Google Scholar 

  77. 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

    Article  Google Scholar 

  78. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. 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

    CAS  Article  Google Scholar 

  80. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  81. 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

    Article  Google Scholar 

  82. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  83. R Core Team (2018) A language and environment for statistical computing

  84. 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

    Article  Google Scholar 

  85. 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

    Article  Google Scholar 

  86. 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

    Article  Google Scholar 

  87. 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

    Article  Google Scholar 

  88. 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

    Article  Google Scholar 

  89. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. 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

    Article  Google Scholar 

  91. 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

    CAS  Article  Google Scholar 

  92. 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

    Article  PubMed  PubMed Central  Google Scholar 

  93. Shenkar N, Swalla BJ (2011) Global diversity of Ascidiacea. PLoS ONE 6:e20657. https://doi.org/10.1371/journal.pone.0020657

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  94. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  95. 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

    Article  Google Scholar 

  96. 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

    Article  Google Scholar 

  97. 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

    Article  Google Scholar 

  98. 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

    Article  Google Scholar 

  99. Stoecker D (1980) Relationships between chemical defense and ecology in benthic ascidians. Mar Ecol Prog Ser 3:257–265

    CAS  Article  Google Scholar 

  100. 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

    Article  Google Scholar 

  101. Tepolt CK (2015) Adaptation in marine invasion: a genetic perspective. Biol Invasions 17:887–903. https://doi.org/10.1007/s10530-014-0825-8

    Article  Google Scholar 

  102. 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

    CAS  Article  PubMed  Google Scholar 

  103. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  104. 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

    Article  Google Scholar 

  105. 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

    Article  Google Scholar 

  106. 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

    CAS  Article  Google Scholar 

  107. 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

    Google Scholar 

  108. 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

    Article  PubMed  PubMed Central  Google Scholar 

  109. 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

    Article  PubMed  PubMed Central  Google Scholar 

  110. 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

    Article  Google Scholar 

  111. Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New York

    Google Scholar 

  112. Wulff JL (1991) Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. J Exp Mar Biol Ecol 149:227–247

    Article  Google Scholar 

  113. 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

    CAS  Article  PubMed  Google Scholar 

  114. Zhan A, Briski E, Bock DG et al (2015) Ascidians as models for studying invasion success. Mar Biol 162:2449–2470

    Article  Google Scholar 

  115. 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

    Article  Google Scholar 

Download references

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).

Author information

Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Marta Pascual.

Ethics declarations

Data accessibility

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.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Ascidians
  • Didemnum vexillum
  • Genotyping-by-sequencing
  • Population genomics
  • Invasive species
  • Whole genome amplification