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Global population genetic structure of the starlet anemone Nematostella vectensis: multiple introductions and implications for conservation policy

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Abstract

Distinguishing natural versus anthropogenic dispersal of organisms is essential for determining the native range of a species and implementing an effective conservation strategy. For cryptogenic species with limited historical records, molecular data can help to identify introductions. Nematostella vectensis is a small, burrowing estuarine sea anemone found in tidally restricted salt marsh pools. This species’ current distribution extends over three coast lines: (i) the Atlantic coast of North America from Nova Scotia to Georgia, (ii) the Pacific coast of North America from Washington to central California, and (iii) the southeast coast of England. The 1996 IUCN Red List designates N. vectensis as “vulnerable” in England. Amplified fragment length polymorphism (AFLP) fingerprinting of 516 individuals from 24 N. vectensis populations throughout its range and mtDNA sequencing of a subsample of these individuals strongly suggest that anthropogenic dispersal has played a significant role in its current distribution. Certain western Atlantic populations of N. vectensis exhibit greater genetic similarity to Pacific populations or English populations than to other western Atlantic populations. At the same time, F-statistics showing high degrees of genetic differentiation between geographically proximate populations support a low likelihood for natural dispersal between salt marshes. Furthermore, the western Atlantic harbors greater genetic diversity than either England or the eastern Pacific. Collectively, these data clearly imply that N. vectensis is native to the Atlantic coast of North America and that populations along the Pacific coast and in England are cases of successful introduction.

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References

  • Amsellem L, Noyer JL, Le Bourgeois T, Hossaert-Mckey M (2000) Comparison of genetic diversity of the invasive weed Rubus alceifolius Poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:443–455

    Article  PubMed  CAS  Google Scholar 

  • Anon (1995) Biodiversity: the UK Steering Group Report. HMSO, London

    Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Bachelet G, Simon-Bouhet B, Desclaux C et al (2004) Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea: origin and effects on resident fauna. Mar Ecol Prog Ser 276:147–159

    Article  Google Scholar 

  • Barnhart RA, Boyd MJ, Pequegnat JE (1992) The ecology of Humboldt Bay, California: an estuarine profile. U.S. Fish and Wildlife Service. Biological Bulletin, vol 1

  • 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 

  • Bensch S, Åkesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914

    Article  PubMed  CAS  Google Scholar 

  • Berg DA, Garton DW, Macisaac HJ, Panov VE, Telesh IV (2002) Changes in genetic structure of North American Bythotrophes populations following invasion from Lake Lagoda, Russia. Freshw Biol 47:275–282

    Article  Google Scholar 

  • Bertness MD, Ewanchuk PJ, Silliman BR (2002) Anthropogenic modification of New England salt marsh landscapes. Proc Natl Acad Sci USA 99:1395–1398

    Article  PubMed  CAS  Google Scholar 

  • Block BA, Teo SLH, Walli A et al (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434:1121–1127

    Article  PubMed  CAS  Google Scholar 

  • Bohonak AJ (2002) IBD (Isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  PubMed  CAS  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Brown JS, Eckert CG (2005) Evolutionary increase in sexual and clonal reproductive capacity during biological invasion in an aquatic plant Butomus umbellatus (Butomaceae). Am J Bot 9:495–502

    Article  Google Scholar 

  • Darling JA, Reitzel AM, Finnerty JR (2004) Regional population structure of a widely introduced estuarine invertebrate: Nematostella vectensis Stephenson in New England. Mol Ecol 13:2969–2981

    Article  PubMed  CAS  Google Scholar 

  • Darling JA, Reitzel AM, Burton P et al (2005) A starlet in the mud: the starlet sea anemone Nematostella vectensis. BioEssays 27:211–221

    Article  PubMed  CAS  Google Scholar 

  • Dawson MN, Sen Gupta A, England MN (2005) Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proc Natl Acad Sci USA 102:11968–11973

    Article  PubMed  CAS  Google Scholar 

  • Donlan J (2005) Re-wilding North America. Nature 436:913–914

    Article  PubMed  CAS  Google Scholar 

  • Eckert CG, Lui K, Bronson K, Corradini P, Bruneau A (2003) Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Mol Ecol 12:331–344

    Article  PubMed  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • 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

    PubMed  CAS  Google Scholar 

  • Frank PG, Bleakney JS (1978) Asexual reproduction, diet, and anomalies of the anemone Nematostella vectensis in Nova Scotia. Can Field Nat 92:259–263

    Google Scholar 

  • Geller JB (1996) Molecular approaches to the study of marine biological invasions. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies, and protocols. Wiley-Liss, New York, pp 119–132

    Google Scholar 

  • Gouin N, Grandjean F, Bouchon D, Reynolds JD, Souty-Grosset C (2001) Population genetic Structure of the endangered freshwater crayfish Austropotamobius pallipes, assessed using RAPD markers. Heredity 87:80–87

    Article  PubMed  CAS  Google Scholar 

  • Grapputo A, Boman S, Lindström L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219

    Article  PubMed  CAS  Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasions a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  • Hand C (1957) Another sea anemone from California and the types of certain California species. J Wash Acad Sci 47:411–414

    Google Scholar 

  • Hand C, Uhlinger K (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 182:169–176

    Article  Google Scholar 

  • Hand C, Uhlinger K (1994) The unique, widely distributed, estuarine sea anemone, Nematostella vectensis Stephenson: a review, new facts and questions. Estuaries 17:501–508

    Article  Google Scholar 

  • Harter VL (1997) The use of Nematostella vectensis Stephenson in aquatic toxicity bioassays: setting the ground work. Masters of Science Thesis, Western Washington University

  • Harter VL, Matthews RA (2005) Acute and chronic toxicity test methods for Nematostella vectensis Stephenson. Bull Environ Contam Toxicol 74:830–836

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann RJ (1986) Variation in contributions of asexual reproduction to the genetic structure of populations of the sea anemone Metridium senile. Evolution 40:357–365

    Article  Google Scholar 

  • Hutchins E, Catena J, James-Pirri MJ (2001) Argilla road salt marsh restoration, Ipswich, Massachusetts. NOAA Restoration Center Project Fact Sheet. National Marine Fisheries Service, Gloucester, MA

  • Kneib RT (1988) Testing for indirect effects of predation in an intertidal soft-bottom community. Ecology 69:1795–1805

    Article  Google Scholar 

  • Kozloff EN (1983) Seashore life of the northern Pacific coast: an illustrated guide to Northern California, Oregon, Washington and British Columbia. University of Washington Press, Seattle

    Google Scholar 

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

    Article  Google Scholar 

  • Li W, Wang B, Wang J (2006) Lack of genetic variation of an invasive clonal plant Eichhornia crassipes in China revealed by RAPD and ISSR markers. Aquat Bot 84:176–180

    Article  CAS  Google Scholar 

  • Lui K, Thompson FL, Eckert CG (2005) Causes and consequences of extreme variation in reproductive strategy and vegetative growth among invasive populations of a clonal aquatic plant, Butomus umbellatus L. (Butomaceae). Biol Invasions 7:427–444

    Article  Google Scholar 

  • McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126

    Article  Google Scholar 

  • Mitchell R (1974) Aspects of the ecology of the lamellibranch Mercenaria mercenaria (L.) in British waters. Hydrobiol Bull 8:124–138

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Nixon SW, Oviatt CA (1973) Ecology of a New England salt marsh. Ecol Monogr 43:463–498

    Article  Google Scholar 

  • Nobrega R, Sole-Cava AM, Russo CAM (2004) High genetic homogeneity of an intertidal marine invertebrate along 8000 km of the Atlantic coast of the Americas. J Exp Mar Biol Ecol 303:173–181

    Article  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

    Article  Google Scholar 

  • Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19

    Article  Google Scholar 

  • Pauchard A, Shea K (2006) Integrating the study of non-native plants invasions across spatial scales. Biol Invasions 8:399–413

    Article  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 

  • Pearson CVM, Rogers AD, Sheader M (2002) The genetic structure of the rare lagoonal sea anemone, Nematostella vectensis Stephenson (Cnidaria; Anthozoa) in the United Kingdom based on RAPD analysis. Mol Ecol 11:2285–2293

    Article  PubMed  CAS  Google Scholar 

  • Posey MH, Hines AH (1991) Complex predator-prey interactions within an estuarine benthic community. Ecology 72:2155–2169

    Article  Google Scholar 

  • Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721

    Article  Google Scholar 

  • Reitzel AM, Burton P, Krone C, Finnerty JR (2007) Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis (Stephenson): embryogenesis, regeneration, and two forms of asexual fission. Invertebr Biol 126:99–112

    Article  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader's range. Proc Biol Sci 273(1600):2453–2459

    Article  PubMed  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 

  • Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2988

    Article  PubMed  CAS  Google Scholar 

  • Rudy P, Rudy LH (1983) Oregon estuarine invertebrates: an illustrated guide to the common and important invertebrate animals. U.S. Fish and Wildlife Service, Washington

    Google Scholar 

  • Ruiz GM, Fofonoff P, Hines AH (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972

    Article  Google Scholar 

  • Ruiz GM, Fofonoff P, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis, Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva

  • Sheader M, Suwailem AM, Rowe GA (1997) The anemone, Nematostella vectensis, in Britain: considerations for conservation management. Aquat Conserv: Mar Freshw Ecosyst 7:13–25

    Article  Google Scholar 

  • Shearer TL, van Oppen JH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487

    Article  PubMed  CAS  Google Scholar 

  • Stephenson TA (1935) The British sea anemones, vol II. The Ray Society, London

    Google Scholar 

  • Stocks KI, Grassle JF (2001) Effects of microalgae and food limitation on the recolonization of benthic macrofauna into in situ saltmarsh-pond mesocosms. Mar Ecol Prog Ser 221:93–104

    Article  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Timmermans MJTN, Ellers J, Mariën J et al (2005) Genetic structure in Orchesella cincta (Collembola): strong subdivision of European populations inferred from mtDNA and AFLP markers. Mol Ecol 14:2017–2024

    Article  PubMed  CAS  Google Scholar 

  • Ting JH, Geller JB (2000) Clonal diversity in introduced populations of an Asian sea anemone in North America. Biol Invasions 2:23–32

    Article  Google Scholar 

  • Uthicke S, Conand C (2005) Amplified fragment length polymorphism (AFLP) analysis indicates the importance of both asexual and sexual reproduction in the fissiparous holothurian Stichopus chloronotus (Aspidochirotida) in the Indian and Pacific Ocean. Coral Reefs 24:103–111

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Vrijenhoek RC (1998) Clonal organisms and the benefits of sex. In: Carvalho G (ed) Advances in molecular ecology. IOS Press, Amsterdam, pp 151–172

    Google Scholar 

  • Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JC (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol Conserv 102:143–153

    Article  Google Scholar 

  • Williams RB (1976) Conservation of the sea anemone Nematostella vectensis in Norfolk, England and its world distribution. Trans Norfolk Norwich Nat Soc 23:257–266

    Google Scholar 

  • Williams RB (1983) The starlet sea anemone: Nematostella vectensis Stephenson 1935. In: Wells SM, Pyle RM, Collins NM (eds) The IUCN invertebrate red data book. International Union for Conservation of Nature and Natural Resources, Gland, pp 43–46

    Google Scholar 

  • Williams RB (1987) The current status of the sea anemone Nematostella vectensis in England. Trans Norfolk Norwich Nat Soc 27:371–374

    Google Scholar 

  • Yonge CM (1960) Oysters. Collins, London

    Google Scholar 

  • Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913

    Article  PubMed  CAS  Google Scholar 

  • Zilberberg C, Solé-Cava AM, Klautau K (2006) The extent of asexual reproduction in sponges of the genus Chondrilla (Demospongiae: Chondrosida) from the Caribbean and the Brazilian coasts. J Exp Mar Biol Ecol 336:211–220

    Article  Google Scholar 

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Acknowledgments

We are extremely grateful to Michael Mazurkiewicz, Wayne Fields, Shawn Arellano, Bruno Pernet, Tammy McGovern, and Kostas Kaltsas for supplying N. vectensis to this study. AMR would also like to thank W and J Reitzel for collection assistance in Nova Scotia. We would like to acknowledge The Trustees of Reservations, Massachusetts and Northeast Regional Ecologist Franz Ingelfinger for access to protected marshes and collection assistance. The Center for Ecology and Conservation Biology (Boston University) partially funded costs associated with collection of samples. AMR was supported by a project AWARE grant. This research was also supported by NSF grant FP-91656101-0 to JCS and JRF, EPA grant F5E11155 to AMR and JRF, and NSF grant IBN-0212773 to JRF.

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Correspondence to John R. Finnerty.

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Reitzel, A.M., Darling, J.A., Sullivan, J.C. et al. Global population genetic structure of the starlet anemone Nematostella vectensis: multiple introductions and implications for conservation policy. Biol Invasions 10, 1197–1213 (2008). https://doi.org/10.1007/s10530-007-9196-8

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