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Long-term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri

Abstract

The accelerated pace of marine biological invasions raises questions pertaining to genetic traits and dynamics underlying the successful establishment of invasive species. Current research stresses the importance of multiple introductions and prolonged gene flow as the main sources for genetic diversity, which, along with genetic drift, affect invasive species success. We here attempt to determine the relative contribution of gene flow and mutation rates as sources of genetic variability using the invasive tunicate Botryllus schlosseri as a model. The study was performed over a 13-year period in the Santa Cruz Harbor, California. With a characteristic life history of five generations/year, the Santa Cruz Botryllus population has already experienced approximately 155 generations since the onset of its invasion. The results (278 specimens, 127 scored alleles, five microsatellite loci) support limited gene flow rate (2.89 × 10−3) and relative genetic isolation. Furthermore, the study population was found to be influenced by both, genetic drift and a high mutation rate (2.47 × 10−2). These findings were supported by high fluctuations in the frequencies of microsatellite alleles, the appearance of new alleles and the loss of others. The balance between genetic drift and a high mutation rate is further elucidated by the high, stable level of genetic variation. We suggest that rapid mutation rates at the microsatellite loci reflect genome-wide phenomena, helping to maintain high genetic variability in relatively isolated populations. The potential adaptability to new environments is discussed.

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References

  1. Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Philos Trans R Soc Lond B Biol Sci 353:177–186

    PubMed  Article  CAS  Google Scholar 

  2. Ben-Shlomo R, Douek J, Rinkevich B (2001) Heterozygote deficiency and chimerism in remote populations of a colonial ascidian from New Zealand. Mar Ecol Prog Ser 209:109–117

    Article  Google Scholar 

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

    Article  Google Scholar 

  4. Ben-Shlomo R, Motro U, Paz G, Rinkevich B (2008) Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri. Genetica 132:51–58

    PubMed  Article  Google Scholar 

  5. Ben-Shlomo R, Reem E, Douek J, Rinkevich B (2010) Population genetics of the invasive ascidian Botryllus schlosseri from South American coasts. Mar Ecol Prog Ser 412:85–92

    Article  Google Scholar 

  6. Bernier YR, Locke A, Hanson JM (2009) Lobsters and crabs as potential vectors for tunicate dispersal in the southern gulf of St. Lawrence, Canada. Aquat Invas 4:105–110

    Article  Google Scholar 

  7. Berrill NJ (1950) The Tunicata with an account of the British species. Ray Society, London

    Google Scholar 

  8. Bock DG, Zahn A, Lejeusne C, Macisaac HJ, Cristescu ME (2011) Looking at both sides of the invasion: patterns of colonization in the violet tunicate Botrylloides violaceus. Mol Ecol 20:503–516

    PubMed  Article  CAS  Google Scholar 

  9. Chadwick-Furman NE, Weissman IL (1995) Life histories and senescence of Botryllus schlosseri (Chordata, Ascidiacea) in Monterey bay. Biol Bull 189:36–41

    PubMed  Article  CAS  Google Scholar 

  10. Cockerham CC, Weir BS (1993) Estimation of gene flow from F-statistics. Evolution 47:855–863

    Article  Google Scholar 

  11. Cohen AN, Carlton JT (1995) Nonindigenous 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 D.C. and the national sea grant college program connecticut sea grant, pp 112, 117

  12. Corander J, Marttinen P, Sirén J, Tang J (2009) BAPS: Bayesian analysis of population. Structure version 5.3. Department of Mathematics, Åbo Akademi University Finland, 27 pp. Available from http://web.abo.fi/fak/mnf/mate/jc/software/BAPS5manual.pdf

  13. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    PubMed  Article  Google Scholar 

  14. Crow JF, Aoki K (1984) Group selection for a polygenic behavioral trait: estimating the degree of population subdivision. Proc Natl Acad Sci USA 81:6073–6077

    PubMed  Article  CAS  Google Scholar 

  15. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    PubMed  Article  CAS  Google Scholar 

  16. Durka W, Bossdorf O, Prati D, Auge H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706

    PubMed  Article  Google Scholar 

  17. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  18. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385

    PubMed  Article  CAS  Google Scholar 

  19. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393

    Article  Google Scholar 

  20. Genton BJ, Shykoff A, Giraud T (2005) High genetic diversity in French invasive populations of common ragweed, Ambrosia artemistiifolia, as a result of multiple sources of introduction. Mol Ecol 14:4275–4285

    PubMed  Article  CAS  Google Scholar 

  21. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852

    PubMed  Article  Google Scholar 

  22. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available http://www2.unil.ch/popgen/softwares/fstat.htm

  23. Graham DE (1978) The isolation of high molecular weight DNA from whole organisms or large tissue masses. Anal Biochem 85:609–613

    PubMed  Article  CAS  Google Scholar 

  24. Grapputo A, Bisazza A, Pilastro A (2006) Invasion success despite reduction of genetic diversity in the European populations of eastern mosquitofish (Gambusia holbruki). Ital J Zool 73:67–73

    Article  CAS  Google Scholar 

  25. Grosberg RK (1987) Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41:372–384

    Article  Google Scholar 

  26. Grosberg RK (1988) Life history variation within a population of a colonial ascidian Botryllus schlosseri, I. The genetic and environmental control of seasonal variation. Evolution 42:900–920

    Article  Google Scholar 

  27. Han YS, Sun YL, Sun YF, Liao YF, Liao IC, Shen KN, Tzeng WN (2008) Temporal analysis of population genetic composition in the overexploited Japanes eel Anguilla japonica. Mar Biol 155:613–621

    Article  Google Scholar 

  28. Harrison XA, Bearhop S, Iinger R, Colhoun K, Gudmundsson GA, Hodgson D, McElwaine G, Tregenza T (2011) Heterozygosity–fitness correlations in a migratory bird: an analysis of inbreeding and single-locus effects. Mol Ecol 20:4786–4795

    PubMed  Article  Google Scholar 

  29. Hartl DL, Clark AG, (1997) Principles of population genetics. Sinauer Associates Inc. Sunderland, MA, pp 289–290

  30. Hedrick PW (2005a) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  31. Hedrick PW (2005b) Genetics of populations. Jones and Bartlet Publishers, Sudbury, MA, pp 501–502

  32. Heller R, Siegismund HR (2009) Relationship between three measures of genetic differentiation GST, DEST and G’ST: how wrong have we been? Mol Ecol 18:2080–2083

    PubMed  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Holland BS (2001) Invasion without a bottleneck: microsatellite variation in natural and invasive populations of the brown mussel, Perna perna (L). Mar Biotechnol 3:407–415

    PubMed  Article  CAS  Google Scholar 

  35. Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429

    PubMed  Article  CAS  Google Scholar 

  36. Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

    PubMed  Article  CAS  Google Scholar 

  37. Johnson RN, Starks PT (2004) A surprising level of genetic diversity in an invasive wasp:Polistes dominulus in the northeastern United States. Ann Entomolog Soc Am 97:732–737

    Article  Google Scholar 

  38. Johnson SL, Yund PO (2007) Variation in multiple paternity in natural populations of a free spawning marine invertebrate. Mol Ecol 16:3253–3262

    PubMed  Article  CAS  Google Scholar 

  39. Jorde PE, Ryman N (1996) Demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies. Genetics 143:1369–1381

    PubMed  CAS  Google Scholar 

  40. Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935

    PubMed  Article  Google Scholar 

  41. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    PubMed  Article  Google Scholar 

  42. Jost L (2009) D vs. Gst: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

    Article  Google Scholar 

  43. Karlsson S, Mork J (2005) Deviation from Hardy-Weinberg equilibrium, and temporal instability in allele frequencies at microsatellite loci in a local population of Atlantic cod. ICES J Mar Sci 62:1588–1596

    Article  CAS  Google Scholar 

  44. Kashi Y, King DG (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22:253–259

    PubMed  Article  CAS  Google Scholar 

  45. Kolbe JJ, Glor RE, Schettino LR, Ada Chamizo L, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    PubMed  Article  CAS  Google Scholar 

  46. 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 

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

    Article  Google Scholar 

  48. Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of southern California bight. Mar Ecol Prog Ser 259:145–161

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  50. Li YC, Korol AB, Fahima T, Beilis A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    PubMed  Article  CAS  Google Scholar 

  51. Light SF (1954) Intertidal Invertebrates of the Central California Coast: S.F. Light’s Laboratory and field text in invertebrate zoology, 2nd edn. (Revised by Smith RI, Pitelka FA, Abbott DO, Weesner FM). University of California Press, CA, USA

  52. Light SF, Smith RI, Carlton JT (1975) Light’s Manual: Intertidal Invertebrates of the Central California Coast: S. F. Light’s Laboratory and field text in invertebrate zoology, 3rd edn. Fourth printing, corrected and updated. University of California Press, CA, USA

  53. Ljungqvist M, Åkesson M, Hansson B (2010) Do microsatellites reflect genome-wide genetic diversity in natural populations? A comment on Väli et al. (2008). Mol Ecol 19:851–855

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  55. Luquet E, David P, Lena JP, Joly P, Konecny L, Dufresnes C, Perrin N, Plenet S (2011) Heterozygosity–fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load. Mol Ecol 20:1877–1887

    PubMed  Article  CAS  Google Scholar 

  56. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18

    PubMed  Article  Google Scholar 

  57. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    PubMed  CAS  Google Scholar 

  58. Miller MP (1997) Tools for population genetic analyses (Tfpga), version 1.3. Department of Biological Sciences, Northern Arizona University, Flagstaff (AZ)

  59. Montgomery ME, Woodworth LM, England PR, Briscoe DA, Frankham R (2010) Widespread selective sweeps affecting microsatellites in Drosophila populations adapting to captivity: implications for captive breeding programs. Biol Conserv 143:1842–1849

    Article  Google Scholar 

  60. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451

    PubMed  Article  CAS  Google Scholar 

  61. Novak SJ (2007) The role of evolution in the invasion process. Proc Natl Acad Sci USA 104:3671–3672

    PubMed  Article  CAS  Google Scholar 

  62. Pancer Z, Gershon H, Rinkevich B (1994) Direct typing of microsatellites in the colonial tunicate Botryllus schlosseri (Ascidiacea). Biochem Bioph Res Co 203:646–651

    Article  CAS  Google Scholar 

  63. Paz G, Douek J, Caiquing M, 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 

  64. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  65. Pérez-Portela R, Turon X, Bishop JDD (2012) Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Mar Ecol Prog Ser 451:93–105

    Google Scholar 

  66. Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333

    Article  Google Scholar 

  67. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  68. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    PubMed  CAS  Google Scholar 

  69. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  70. Rinkevich B (2005) Natural chimerism in colonial Urochordates. J Exp Mar Biol Ecol 322:93–109

    Article  Google Scholar 

  71. Rinkevich B, Weissman IL (1987) The fate of Botryllus (Ascidiacea) larvae cosettled with parental colonies: beneficial or deleterious consequences? Biol Bull 173:474–488

    Article  Google Scholar 

  72. Rinkevich B, Porat R, Goren M (1995) Allorecognition elements on a urochordate histocompatibility locus indicate unprecedented extensive polymorphism. Proc R Soc Lond B 259:319–324

    Article  Google Scholar 

  73. Rinkevich B, Paz G, Douek J, Ben-Shlomo R (2001) Allorecognition and microsatellite allele polymorphism of Botryllus schlosseri from the Adriatic Sea. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of Ascidians. Springer, Tokyo, pp 426–435

    Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  76. Ruiz GM, Huber T, Larson K, McCann L, Steves B, Fofonoff P, Hines AH (2006) Biological invasions in Alaska’s coastal marine ecosystems: establishing a baseline. Smithsonian Environmental Research Center Edgewater, Maryland, USA

    Google Scholar 

  77. Ryman N, Leimar O (2009) GST is still a useful measure of differentiation -a comment on Jost’s D. Mol Ecol 18:2084–2087

    PubMed  Article  Google Scholar 

  78. 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 

  79. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  80. Stepien CA, Brown JE, Neilson ME, Tumeo MA (2005) Genetic diversity of invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Anal 25:1043–1060

    PubMed  Article  Google Scholar 

  81. Stoner DS, Quattro JM, Weissman IL (1997) Highly polymorphic microsatellite loci in the colonial ascidian Botryllus schlosseri. Mol Mar Biol Biotech 6:163–171

    CAS  Google Scholar 

  82. 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 

  83. Strelow Consulting In association with Santa Cruz Port District (2009) Final Santa Cruz Harbor dredge management plan, pp 2–2, 3–3. Available from www.santacruzharbor.org

  84. Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360

    PubMed  Article  Google Scholar 

  85. Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken, NJ, pp 56–58

  86. Templeton AR (2008) The reality and importance of founder speciation in evolution. BioEssays 30:470–479

    PubMed  Article  Google Scholar 

  87. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953

    PubMed  Article  CAS  Google Scholar 

  88. Väli Ü, Einarsson A, Waits L, Ellegren H (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17:3808–3817

    PubMed  Article  Google Scholar 

  89. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  91. Ward SM, Gaskin JF, Wilson LM (2008) Ecological genetics of plant invasion: what do we know? Invasive Plant Sci Manage 1:98–109

    Article  Google Scholar 

  92. Xu H, Fu YX (2004) Estimating effective population size or mutation rate with microsatellites. Genetics 166:555–563

    PubMed  Article  CAS  Google Scholar 

  93. Yund PO, Feldgarden M (1992) Rapid proliferation of historecognition alleles in populations of a colonial Ascidian. J Exp Zool 263:442–452

    Article  CAS  Google Scholar 

  94. Zayed A, Constantin ŞA, Packer L (2007) Successful Biological invasion despite a severe genetic load. PLoS ONE 2:e868. doi:10.1371/journal.pone.0000868

    PubMed  Article  Google Scholar 

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Acknowledgments

We thank Alan Templeton and Per Erik Jorde for their constructive remarks and suggestions on earlier drafts. Daniel Reem for help with data analysis, Tim Morley from Santa Cruz Harbor for helpful information and Guy Paz for technical help and figure preparation. This study is part of the PhD dissertation of E. Reem and was supported by grants from the Israel Science Foundation (1342/08 and 68/10).

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Correspondence to Eitan Reem.

Appendix

Appendix

See Table 4.

Table 4 Allele frequencies and sample size by populations (sample size = number of individuals per loci)

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Reem, E., Douek, J., Katzir, G. et al. Long-term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri . Biol Invasions 15, 225–241 (2013). https://doi.org/10.1007/s10530-012-0281-2

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Keywords

  • Genetic diversity
  • Genetic drift
  • Invasions
  • Microsatellites
  • Mutations