Skip to main content
SpringerLink
Log in

Lineage distribution and barriers to gene flow among populations of the globally invasive marine mussel Musculista senhousia

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

Abstract

Introduced species seem to rapidly adapt to non-native conditions although founder events may decrease genetic variance and impede adaptation. Cryptic introductions of an invader from different parts of its native range may allow colonization of habitat patches with compatible conditions, or admixture may restore genetic diversity lost during invasion bottlenecks. We present the first genetic study of global invasion pathways for the Asian date mussel, Musculista senhousia, comparing three putative source populations from Asia with six US estuaries and one invaded site in New Zealand and the Mediterranean Sea, totaling 117 individuals. Distribution of mitochondrial DNA and alleles of a nuclear intron revealed two genetically divergent populations in the native range. A warm-water lineage from Tokyo Bay and southwestern South Korea predominated in southern California and New Zealand, while a cold-water haplotype group sampled in northeastern Korea was more abundant at invaded sites in the northwestern US and Mediterranean Sea. The duration of high summer water temperatures accounted for substantial variance in the worldwide distribution of common haplotype groups, suggesting thermal pre-adaptation may influence invasion success for differentiated source populations. There was no gene flow across central California, but on either side of this phylogeographic barrier there was high exchange among estuaries within the northern and the southern US regional populations. Gradients in water temperature may therefore constrain post-introduction spread by limiting dispersion along a coast.

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

  • Bastrop R, Blank M (2006) Multiple invasions—a polychaete genus enters the Baltic Sea. Biol Inv 8:1195–1200

    Article  Google Scholar 

  • Carlton JT (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Ph.D. dissertation, UC Davis

  • Carlton JT (1996a) Marine bioinvasions: the alteration of marine ecosystems by nonindigenous species. Oceanography 9:36–43

    Google Scholar 

  • Carlton JT (1996b) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chang YJ, Lim HK, Park YJ (1997) Reproductive cycle of the cultured scallop, Patinopecten yessoensis in eastern waters of Korea. J Aquac 10:133–141

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cohen AN, Carlton JT (1995) Non-indigenous aquatic species in a United States estuary; a case study of the biological invasions of the San Francisco Bay and Delta. United States Fish and Wildlife Service, Washington

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Creese R, Hooker S, De Luca S, Wharton Y (1997) Ecology and environmental impact of Musculista senhousia (Mollusca: Bivalvia: Mytilidae) in Tamaki Estuary, Auckland, New Zealand. N Z J Mar Fresh Res 31:225–236

    Article  Google Scholar 

  • Crooks JA (1996) The population ecology of an exotic mussel, Musculista senhousia, in a southern California bay. Estuaries 19:42–50

    Article  Google Scholar 

  • Crooks JA (2001) Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon. Biol Inv 3:23–26

    Article  Google Scholar 

  • Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75

    Article  Google Scholar 

  • Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeogr 28:723–736

    Article  Google Scholar 

  • Ellingson RA, Krug PJ (2006) Evolution of poecilogony from planktotrophy: cryptic speciation, phylogeography, and larval development in the gastropod genus Alderia. Evolution 60:2293–2310

    PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA 7 restriction data. Genetics 131:479–491

    PubMed  CAS  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  Google Scholar 

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

    CAS  Google Scholar 

  • Frankham R (2005) Invasion biology—resolving the genetic paradox in invasive species. Heredity 94:385

    Article  PubMed  CAS  Google Scholar 

  • Fu Y, Li W (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Geller JB (1999) Decline of a native mussel masked by sibling species invasion. Conserv Biol 13:661–664

    Article  Google Scholar 

  • Geller JB, Carlton JT, Powers DA (1994) PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion. Mar Biol 119:243–249

    Article  CAS  Google Scholar 

  • Geller JB, Sotka EE, Kado R, Palumbi S, Schwindt E (2008) Sources of invasions of a northeastern Pacific acorn barnacle, Balanus glandula, in Japan and Argentina. Mar Ecol Prog Ser 358:211–218

    Article  Google Scholar 

  • Gilman SE, Wethey DS, Helmuth B (2006) Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales. Proc Natl Acad Sci 102:9560–9565

    Article  Google Scholar 

  • Grapputo A, Boman S, Lindstrom 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 

  • Grosholz ED (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B (Suppl) 270:S96–S99

    Article  CAS  Google Scholar 

  • Hickerson MJ, Meyer CP, Moritz C (2006) DNA barcoding will often fail to discover new animal species over broad parameter space. Syst Biol 55:729–739

    Article  PubMed  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Google Scholar 

  • Hoenselaar HJ, Hoenselaar J (1989) Musculista senhousia (Benson in Cantor, 1842) in the Western Mediterranean (Bivalvia., Mytilidae). Basteria 53:73–76

    Google Scholar 

  • Hoffmann R, Boore J, Brown W (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128

    Article  Google Scholar 

  • Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Ishii H, Tanaka F (2001) Food and feeding of Aurelia aurita in Tokyo Bay with an analysis of stomach contents and a measurement of digestion times. Hydrobiologia 451:311–320

    Google Scholar 

  • Jarman S, Ward R, Elliott N (2002) Oligonucleotide primers for PCR amplification of coelomate introns. Mar Biotech 4:347–355

    Article  CAS  Google Scholar 

  • Kimura T, Sekiguchi H (1996) Effects of temperature on larval development of two Mytilid species and their implication. Venus 55:215–222

    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 LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  PubMed  CAS  Google Scholar 

  • Kulikova VA (1978) Morphology, seasonal population dynamics, and settlement of larvae of the bivalve mollusc Musculista senhousia in Busse Lagoon (South Sakhalin). Sov J Mar Biol 4:769–773

    Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • Lavoie DM, Smith LD, Ruiz GM (1999) The potential for intracoastal transfer of non-indigenous species in the ballast water of ships. Estuarine Coast Sci 48:551–564

    Article  Google Scholar 

  • Lee JH (2001) Gonadal development and reproductive cycle of the top shell, Omphalius rusticus (Gastropoda: Trochidae). Korean J Biol Sci 5:37–44

    Article  Google Scholar 

  • Lindholm AK, Breden F, Alexander HJ, Chan W-K, Thakurta SG, Brooks R (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682

    Article  PubMed  CAS  Google Scholar 

  • Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH, Koehn RK (1988) The mussels Mytilus galloprovincialis and M. trossulus on the Pacific coast of North America. Mar Biol 99:111–118

    Article  Google Scholar 

  • Mikkelsen NT, Schander C, Willassen E (2007) Local scale DNA barcoding of bivalves (Mollusca): a case study. Zool Scripta 36:455–463

    Article  Google Scholar 

  • Mistri M (2003) The non-indigenous mussel Musculista senhousia in an Adriatic lagoon: effects on benthic community over a ten year period. J Mar Biol Assoc UK 83:1277–1278

    Article  Google Scholar 

  • Mistri M (2004) Predatory behavior and preference of a successful invader, the mud crab Dyspanopeus sayi (Panopeidae), on its bivalve prey. J Exp Mar Biol Ecol 312:385–398

    Article  Google Scholar 

  • Morton B (1974) Some aspects of the biology, population dynamics, and functional morphology of Musculista senhausia Benson (Bivalvia, Mytilidae). Pac Sci 28:19–33

    Google Scholar 

  • Nylander JAA (2004) MrModeltest. Program distributed by the author, Uppsala

  • Passamonti M (2007) An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca: Bivalvia). BMC Evol Biol 7:S2–S7

    Article  Google Scholar 

  • Posada D (2004) Collapse ver. 1.2. Available from http://darwin.uvigo.es

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. University Press, Cambridge

    Google Scholar 

  • Reusch TBH, Williams SL (1998) Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia. Oecologia 113:428–441

    Article  Google Scholar 

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

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

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Ann Rev Ecol Syst 36:643–689

    Article  Google Scholar 

  • Ruiz GM, Crooks JA (2001) Marine invaders: patterns, effects, and management of non-indigenous species. In: Gallagher P, Bendell-Young L (eds) Waters in Peril. Kluwer Academic Publishers, Norwell

    Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: Mechanisms, extent, and consequences. Am Zool 37:621–632

    Google Scholar 

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

    Article  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Schmidt PS, Bertness MD, Rand DM (2000) Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides. Proc R Soc Lond B 267:379–384

    Article  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

    Google Scholar 

  • Simmons MP, Pickett KM, Miya M (2004) How meaningful are Bayesian support values? Mol Biol Evol 21:188–199

    Article  PubMed  CAS  Google Scholar 

  • Simon-Bouhet B, Garcia-Meunier P, Viard F (2006) Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France: evidence from mitochondrial sequence data. Mol Ecol 15:1699–1711

    Article  PubMed  CAS  Google Scholar 

  • Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156

    Article  PubMed  CAS  Google Scholar 

  • Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates non-indigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500

    Article  PubMed  CAS  Google Scholar 

  • Städler T, Frye M, Neiman M, Lively CM (2005) Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail. Mol Ecol 14:2465–2473

    Article  PubMed  Google Scholar 

  • Staubitz WW, Bortleson GC, Semans SD, Tesoriero AJ, Black RW (1997) Water-quality assessment of the Puget Sound Basin, Washington—environmental setting and its implications for water quality and aquatic biota. US geological survey water-resources investigations report 97-4013

  • Stepien CA, Tumeo MA (2006) Invasion genetics of Ponto-Caspian gobies in the Great Lakes: a “cryptic” species, absence of founder effects, and comparative risk analysis. Biol Inv 8:68–78

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc Acid Res 24:4876–4882

    Article  Google Scholar 

  • Uddin MJ, Park K-I, Kang D-H, Park Y-J, Choi K-S (2007) Comparative reproductive biology of Yezo scallop, Patinopecten yessoensis, under two different culture systems on the east coast of Korea. Aquaculture 265:139–147

    Article  Google Scholar 

  • Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci 102:5432–5437

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Willan RC (1985) Successful establishment of the Asian mussel Musculista senhousia (Benson in Cantor, 1842) in New Zealand. Records Auckl Inst Mus 22:85–96

    Google Scholar 

  • Willan RC (1987) The mussel Musculista senhousia in Australasia; another aggresive alien highlights the need for quarantine at ports. Bull Mar Sci 41:475–789

    Google Scholar 

  • Zaldivar JM, Cattaneo E, Plus M, Murray CN, Giordani G, Viaroli P (2003) Long-term simulation of main biogeochemical events in a coastal lagoon: Sacca Di Goro (Northern Adriatic coast, Italy). Cont Shelf Res 23:1847–1875

    Article  Google Scholar 

Download references

Acknowledgments

We thank J. Crooks for inspiring this study and for collection help, W. Blom and M. Morley for specimens from New Zealand, and S. Williams, A. Cohen, and M. Boyd for assistance with field sites. Special thanks to M. Owada for collecting Asian specimens. Access to field sites was provided by I. Kay of the Natural Reserve Office, University of California (Mission Bay, CA), B. Shelton and Jeff Stoddard (Upper Newport Bay Ecological Reserve), and M. Schaadt (Cabrillo Aquarium, Los Angeles). We thank J. Carlton, S. Palumbi and anonymous reviewers for comments that greatly improved the paper. This study was supported by awards to PJK from the US National Science Foundation (awards OCE 06-48606 and 11-30072, DEB 08-17084, and HRD 03-17772), a faculty-student collaborative grant from the California State University Program for Education and Research in Biotechnology (CSUPERB), and an NSF GK-12 fellowship to J. Asif.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, California State University, 5151 State University Drive, Los Angeles, CA, 90032-8201, USA

    Jamal H. Asif & Patrick J. Krug

Authors
  1. Jamal H. Asif
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick J. Krug
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick J. Krug.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Asif, J.H., Krug, P.J. Lineage distribution and barriers to gene flow among populations of the globally invasive marine mussel Musculista senhousia . Biol Invasions 14, 1431–1444 (2012). https://doi.org/10.1007/s10530-011-0169-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-0169-6

Keywords

Search

Navigation