Skip to main content

Advertisement

SpringerLink
Log in

Comparative phylogeography of two colonial ascidians reveals contrasting invasion histories in North America

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Surveys of genetic structure of introduced populations of nonindigenous species may reveal the source(s) of introduction, the number of introduction events, and total inoculum size. Here we use the mitochondrial cytochrome c oxidase subunit 1 (COI) gene to explore genetic structure and contrast invasion histories of two ecologically similar and highly invasive colonial ascidians, the golden star tunicate Botryllus schlosseri and the violet tunicate Botrylloides violaceus, in their global and introduced North American ranges. Haplotype and nucleotide diversities for B. schlosseri were significantly higher than for B. violaceus both globally (h = 0.872; π = 0.054 and h = 0.461; π = 0.007, respectively) and in their overlapping North American ranges (h = 0.874; π = 0.012 and h = 0.384; π = 0.006, respectively). Comparative population genetics and phylogenetic analyses revealed clear differences in patterns of invasion for these two species. B. schlosseri populations on the west and east coasts of North America were seeded from the Pacific and Mediterranean regions, respectively, whereas all North American B. violaceus populations were founded by one or more introduction events from Japan. Differences in genetic structure of invasive populations for these species in North America are consistent with their contrasting probable introduction vectors. B. schlosseri invasions most likely resulted from vessel hull fouling, whereas B. violaceus was likely introduced as a ‘fellow traveler’ in the shellfish aquaculture trade.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • BCMAL (2007) Shellfish aquaculture: current statistics. British Columbia Ministry of Aquaculture and Lands, BC, 108 pp

    Google Scholar 

  • Ben-Shlomo R, Paz G, Rinkevich B (2006) Postglacial-period and recent invasions shape the population genetics of botryllid ascidians along European Atlantic coasts. Ecosystems 9:1118–1127

    Article  Google Scholar 

  • Berril NJ (1950) The Tunicata, with an account of British species. Ray Society, London, iii+354pp

  • Brunetti R, Beghi L, Bressan M, Marin MG (1980) Combined effects of temperature and salinity on colonies of Botryllus schlosseri and Botrylloides leachi (Ascidiacea) from the Venetian Lagoon. Mar Ecol Prog Ser 2:303–314

    Article  Google Scholar 

  • Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–266

    Article  Google Scholar 

  • Carlton JT (2005) Setting ascidian invasions on the global stage. International Invasive Sea Squirt Conference. Woods Hole Oceanographic Institution, Woods Hole

    Google Scholar 

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

    Article  Google Scholar 

  • Carver CE, Mallet AL, Vercaemer B (2006) Biological synopsis of the colonial tunicates, Botryllus schlosseri and Botrylloides violaceus. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2747: v+42p

  • Castilla JC, Guinez R, Caro AU, Ortiz V (2004) Invasion of a rocky intertidal shore by the tunicate Pyura praeputialis in the Bay of Antofagasta, Chile. Proc Natl Acad Sci 101:8517–8524

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Cohen AN, Carlton JT (1995) Biological study. Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta. A report for the US Fish and Wildlife Service and National Sea Grant College Program. National Technical Information Service, Springfield, p 246

    Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Article  Google Scholar 

  • Colautti RI, Manca M, Viljanen M, Ketelaars HAM, Burgi H, MacIsaac HJ, Heath DD (2005) Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Mol Ecol 14:1869–1879

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Crandall KA (1996) Multiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences. Mol Biol Evol 13:115–131

    CAS  PubMed  Google Scholar 

  • Cristescu MEA, Hebert PDN, Witt JDS, MacIsaac HJ, Grigrovich IA (2001) An invasion history for Cercopagis pengoi based on mitochondrial gene sequences. Limnol Oceanogr 46:224–229

    Article  Google Scholar 

  • Deangelis MM, Wang DG, Hawkins TL (1995) Solid-phase reversible immobilization for the isolation of PCR products. Nucleic Acids Res 23:4742–4743

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra J, Harris LG, Westerman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68

    Article  Google Scholar 

  • Drake JM, Lodge DM (2004) Global hot spots of biological invasions: evaluating options for ballast-water management. Proc R Soc Lond Ser B Biol Sci 271:575–580

    Article  Google Scholar 

  • Dupont L, Viard F, Dowell MJ, Wood C, Bishop JDD (2009) Fine- and regional-scale genetic structure of the exotic ascidian Styela clava (Tunicata) in southwest England, 50 years after its introduction. Mol Ecol 18:442–453

    Article  CAS  PubMed  Google Scholar 

  • Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320

    Article  CAS  Google Scholar 

  • Epelbaum A, Herborg LM, Therriault TW, Pearce CM (2009) Temperature and salinity effects on growth, survival, reproduction, and potential distribution of two non-indigenous botryllid ascidians in British Columbia. J Exp Mar Biol Ecol 369:43–52

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Fay RC, Vallee JA (1979) A survey of the littoral and sublittoral ascidians of southern California, including the Channel Islands. Bull South Calif Acad Sci 70:114–124

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Frankham R (2005) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755

    Article  CAS  PubMed  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  Google Scholar 

  • Gittenberger A (2007) Recent population expansions of non-native ascidians in the Netherlands. J Exp Mar Biol Ecol 342:122–126

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    Article  PubMed  Google Scholar 

  • Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci 102:7198–7202

    Article  CAS  PubMed  Google Scholar 

  • Keane T, Creevey C, Pentony M, Naughton T, Mclnerney J (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LRG, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  CAS  PubMed  Google Scholar 

  • Lambert G (2005) Ecology and natural history of the protochordates. Can J Zool 83:34–50

    Article  Google Scholar 

  • Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4

    Article  Google Scholar 

  • Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688

    Article  Google Scholar 

  • 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 

  • LeBlanc N, Davidson J, Tremblay R, McNiven M, Landry T (2007) The effect of anti-fouling treatments for the clubbed tunicate on the blue mussel, Mytilus edulis. Aquaculture 264:205–213

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • LeGresley M, Martin J, McCurdy P, Thorpe B, Chang B (2008) Non-indigenous tunicate species in the Bay of Fundy, eastern Canada. ICES J Mar Sci 65:770–774

    Article  Google Scholar 

  • Lejeusne C, Chevaldonné P (2006) Brooding crustaceans in a highly fragmented habitat: the genetic structure of Mediterranean marine cave-dwelling mysid populations. Mol Ecol 15:4123–4140

    Article  CAS  PubMed  Google Scholar 

  • Locke A, Hanson JM, Ellis KM, Thompson J, Rochette R (2007) Invasion of the southern Gulf of St. Lawrence by the clubbed tunicate (Styela clava Herdman): potential mechanisms for invasions of Prince Edward Island estuaries. J Exp Mar Biol Ecol 342:69–77

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lopez-Legentil S, Turon X, Planes S (2006) Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Mol Ecol 15:3957–3967

    Article  CAS  PubMed  Google Scholar 

  • May GE, Gelembiuk GW, Panov VE, Orlova MI, Lee CE (2006) Molecular ecology of zebra mussel invasions. Mol Ecol 15:1021–1031

    Article  CAS  PubMed  Google Scholar 

  • McCarthy A, Osman RW, Whitlatch RB (2007) Effects of temperature on growth rates of colonial ascidians: a comparison of Didemnum sp. to Botryllus schlosseri and Botrylloides violaceus. J Exp Mar Biol Ecol 342:172–174

    Article  Google Scholar 

  • Meenakshi VK, Senthamarai S (2006) First report on two species of ascidians to represent the genus Botryllus Gaertner, 1774 from Indian waters. J Mar Biol Assoc India 48:100–102

    Google Scholar 

  • Muirhead J, Gray D, Kelly D, Ellis S, Heath D, MacIsaac H (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:431–449

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pallas PS (1766) Elenchus zoophytorum sistens generum adumbrationes generaliores et specierum cognitarum succinctas descriptiones cum selectis auctorum synomymis. Varrentrapp, F, Frankfurt, p 539

    Google Scholar 

  • Panchal M, Beaumont MA (2007) The automation and evaluation of nested clade phylogeographic analysis. Evolution 61:1466–1480

    Article  PubMed  Google Scholar 

  • Paz G, Douek J, Mo CQ, Goren M, Rinkevich B (2003) Genetic structure of Botryllus schlosseri (Tunicata) populations from the Mediterranean coast of Israel. Mar Ecol Prog Ser 250:153–162

    Article  CAS  Google Scholar 

  • Perez-Portela R, Turon X (2008) Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 111:163–178

    Article  PubMed  Google Scholar 

  • Petit RJ (2007) The coup de grâce for the nested clade phylogeographic analysis? Mol Ecol 17:516–518

    PubMed  Google Scholar 

  • Pfenninger M, Posada D (2002) Phylogeographic history of the snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution 56:1776–1788

    PubMed  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rogers AD, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial. Genetics 152:1079–1089

    CAS  PubMed  Google Scholar 

  • Stoner DS, Ben-Shlomo R, Rinkevich B, Weissman IL (2002) Genetic variability of Botryllus schlosseri invasions to the east and west coasts of the USA. Mar Ecol Prog Ser 243:93–100

    Article  Google Scholar 

  • Suarez AV, Tsutsui ND, Holway DA (1999) Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biol Invasions 1:43–53

    Article  Google Scholar 

  • Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (*and others methods). Sinauer, Sunderland

    Google Scholar 

  • Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809

    Article  PubMed  Google Scholar 

  • Templeton A (2008) Nested clade analysis: an extensively validated method for strong phylogeographic inference. Mol Ecol 17:1877–1880

    Article  PubMed  Google Scholar 

  • Templeton AR (2009) Statistical hypothesis testing in intraspecific phylogeography: nested clade phylogeographical analysis vs. approximate Bayesian computation. Mol Ecol 18:319–331

    Article  PubMed  Google Scholar 

  • Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343–351

    CAS  PubMed  Google Scholar 

  • Valentine PC, Collie JS, Reid RN, Asch RG, Guida VG, Blackwood DS (2007) The occurrence of the colonial ascidian Didemnum sp on Georges Bank gravel habitat—ecological observations and potential effects on groundfish and scallop fisheries. J Exp Mar Biol Ecol 342:179–181

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge our Canadian Aquatic Invasive Species Network (CAISN) colleagues G. Arsenault, J. Davidson, J. Hill, and A. Ramsay as well as our global colleagues T. Bolton, P. Chevaldonné, R. Graille, E. Grey, A. Izquierdo-Munoz, B. de Ligondes, S. Lopez-Legentil, J.-M. Nicolas, M. Ruis-Viladomiu, Y. Saito, X. Turon, and B. Vercaemer, who have so generously provided tunicate samples. D. Heath, S. Xu and A. Zhan provided valuable comments on an early draft of the manuscript. We also thank A. Adebayo, K. Laroche and R. Hepburn for assisting with lab work. This work was supported by CAISN, Fisheries and Oceans Canada and by NSERC Discovery grants to MEC and HJM.

Author information

Authors and Affiliations

  1. Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, N9B 3P4, Canada

    Christophe Lejeusne, Dan G. Bock, Hugh J. MacIsaac & Melania E. Cristescu

  2. Wetland Ecology Department, Estación Biológica de Doñana-CSIC, Avenida Américo Vespucio, s/n, 41092, Sevilla, Spain

    Christophe Lejeusne

  3. Fisheries and Oceans Canada, Pacific Biological Station, Nanaimo, BC, V9T 6N7, Canada

    Thomas W. Therriault

Authors
  1. Christophe Lejeusne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dan G. Bock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas W. Therriault
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hugh J. MacIsaac
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Melania E. Cristescu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hugh J. MacIsaac.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 132 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lejeusne, C., Bock, D.G., Therriault, T.W. et al. Comparative phylogeography of two colonial ascidians reveals contrasting invasion histories in North America. Biol Invasions 13, 635–650 (2011). https://doi.org/10.1007/s10530-010-9854-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9854-0

Keywords

Search

Navigation