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Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata

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Abstract

Increases in temperature can shorten planktonic larval durations, so that higher temperatures may reduce dispersal distances for many marine animals. To test this prediction, we first quantified how minimum time to settlement is shortened at higher temperatures for the ascidian Styela plicata. Second, using latitude as a correlate for ocean temperature and spatial genetic structure as a proxy for dispersal, we tested for a negative correlation between latitude and spatial genetic structure within populations, as measured by anonymous DNA markers. Spatial genetic structure was variable among latitudes, with significant structure at low and intermediate latitudes (high and medium temperatures) and there was no genetic structure within high-latitude (low temperature) populations. In addition, we found consistently high genetic diversity across all Australian populations, showing no evidence for recent local bottlenecks associated S. plicata’s history as an invasive species. There was, however, significant genetic differentiation between all populations indicating limited ongoing gene flow.

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References

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acid Res 25:4692–4693

    Article  PubMed  CAS  Google Scholar 

  • Bay LK, Buechler K, Gagliano M, Caley MJ (2006) Intraspecific variation in the pelagic larval duration of tropical reef fishes. J Fish Biol 68:1206–1214

    Article  Google Scholar 

  • Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Ann Rev Ecol Syst 32:159–181

    Article  Google Scholar 

  • Bingham BL, Young CM (1991) Larval behavior of the ascidian Ecteinascidia turbinata Herdman—an in situ experimental study of the effects of swimming on dispersal. J Exp Mar Biol Ecol 145:189–204

    Article  Google Scholar 

  • Blanquer A, Uriz MJ, Caujape-Castells J (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Mar Ecol Prog Ser 380:95–102

    Article  Google Scholar 

  • Bourque D, Davidson J, MacNair NG, Arsenault G, LeBlanc AR, Landry T, Miron G (2007) Reproduction and early life history of an invasive ascidian Styela clava Herdman in Prince Edward Island, Canada. J Exp Mar Biol Ecol 342:78–84

    Article  Google Scholar 

  • Bradbury IR, Laurel B, Snelgrove PVR, Bentzen P, Campana SE (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc R Soc Biol Sci Ser B 275:1803–1809

    Article  Google Scholar 

  • Calderon I, Ortega N, Duran S, Becerro M, Pascual M, Turon X (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810

    Article  PubMed  Google Scholar 

  • Cloney RA (1982) Ascidian larvae and the events of metamorphosis. Am Zool 22:817–826

    Google Scholar 

  • de Barros RC, da Rocha RM, Pie MR (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquat Inv 4:45–57

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dupont L, Viard F, Bishop JDD (2006) Isolation and characterization of twelve polymorphic microsatellite markers for the invasive ascidian Styela clava (Tunicata). Mol Ecol Notes 6:101–103

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Dupont L, Viard F, Davis MH, Nishikawa T, Bishop JDD (2010) Pathways of spread of the introduced ascidian Styela clava (Tunicata) in Northern Europe, as revealed by microsatellite markers. Biol Invasions. doi:10.1007/s10530-009-9676-0

  • 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

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  PubMed  CAS  Google Scholar 

  • Floerl O, Inglis GJ, Dey K, Smith A (2009) The importance of transport hubs in stepping-stone invasions. J Appl Ecol 46:37–45

    Article  Google Scholar 

  • Galletly BC, Blows MW, Marshall DJ (2007) Genetic mechanisms of pollution resistance in a marine invertebrate. Ecol Appl 17:2290–2297

    Article  PubMed  Google Scholar 

  • Grosberg RK, Quinn RJ (1986) The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322:456–459

    Article  Google Scholar 

  • Hadfield MG, Carpizo-Ituarte EJ, del Carmen K, Nedved BT (2001) Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 41:1123–1131

    Article  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Heller C (1878) Beitrage zur nahern Kenntnis der Tunicaten. Sitzber Akad Wiss Wien 77:2–28

    Google Scholar 

  • Hewitt CL et al (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202

    Article  Google Scholar 

  • Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability, and the development of marine invertebrate larvae. Am Zool 35:415–425

    Google Scholar 

  • Johnson ML, Gaines MS (1990) Evolution of dispersal—theoretical models and empirical tests using birds and mammals. Ann Rev Ecol Syst 21:449–480

    Article  Google Scholar 

  • Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325

    Article  Google Scholar 

  • Kelly RP, Eernisse DJ (2007) Southern hospitality: a latitudinal gradient in gene flow in the marine environment. Evolution 61:700–707

    Article  PubMed  CAS  Google Scholar 

  • Kinlan B, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Article  Google Scholar 

  • Kott P (1985) The Australian Ascidiacea—Phlebobranchia and Stolidobranchia. Mem Queenl Mus 23:1–440

    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 

  • Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Int Comp Biol 46:282–297

    Article  CAS  Google Scholar 

  • López-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  PubMed  CAS  Google Scholar 

  • Marshall DJ (2002) In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate. Mar Ecol Prog Ser 236:113–119

    Article  Google Scholar 

  • Marshall DJ, Pechenik JA, Keough MJ (2003) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial, ascidian Diplosoma listerianum. Mar Ecol Prog Ser 246:153–162

    Article  Google Scholar 

  • McDonald JH, Verrelli BC, Geyer LB (1996) Lack of geographic variation in anonymous nuclear polymorphisms in the American oyster, Crassostrea virginica. Mol Biol Evol 13:1114–1118

    PubMed  CAS  Google Scholar 

  • Miller KJ, Ayre DJ (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol 77:713–724

    Article  PubMed  Google Scholar 

  • O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution and conservation. Proc Natl Acad Sci USA 104:1266–1271

    Article  PubMed  CAS  Google Scholar 

  • Olson RR, McPherson R (1987) Potential vs. realized larval dispersal: fish predation on larvae of the ascidian Lissoclinum patella (Gottschaldt). J Exp Mar Biol Ecol 110:245–256

    Article  Google Scholar 

  • 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 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    PubMed  Google Scholar 

  • Pechenik JA (1990) Delayed metamorphosis by larvae of benthic marine invertebrates: does it occur: is there a price to pay? Ophelia 32:63–94

    Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Gen 6:847–859

    Article  CAS  Google Scholar 

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

    PubMed  CAS  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 

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

    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. Tr Ecol Evol 22:465–471

    Article  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotech 18:233–234

    Article  CAS  Google Scholar 

  • Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385

    PubMed  Google Scholar 

  • Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol App 13:S159–S169

    Article  Google Scholar 

  • Shea DJ, Trenberth KE, Reynolds RW (1992) A global monthly sea-surface temperature climatology. J Clim 5:987–1001

    Article  Google Scholar 

  • Siegal D, Kinlan BP, Gaylord B, Gaines SD (2003) Lagrangian descriptions of marine larval dispersion. Mar Ecol Prog Ser 260:83–96

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Svane IB, Havenhand JN (1993) Spawning and dispersal in Ciona intestinalis (L.). Mar Ecol 14:53–66

    Article  Google Scholar 

  • Svane IB, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceangr Mar Biol Ann Rev 27:45–90

    Google Scholar 

  • Thiyagarajan V, Qian PY (2003) Effect of temperature, salinity and delayed attachment on development of the solitary ascidian Styela plicata (Lesueur). J Exp Mar Biol Ecol 290:133–146

    Article  Google Scholar 

  • Underwood AJ, Fairweather PG (1989) Supply-side ecology and benthic marine assemblages. Tr Ecol Evol 4:16–20

    Article  Google Scholar 

  • Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acid Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Wares JP, Hughes AR, Grosberg R (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax D, Stachowicz J, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer, Sunderland

    Google Scholar 

  • Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Article  Google Scholar 

  • Wellington GM, Victor BC (1992) Regional differences in duration of the planktonic larval stage of reef fishes in the eastern Pacific Ocean. Mar Biol 113:491–498

    Article  Google Scholar 

  • West AB, Lambert CC (1976) Control of spawning in the tunicate Styela plicata by variations in a natural light regime. J Exp Zool 195:263–270

    Article  Google Scholar 

  • Wiens JA (2001) The landscape context of dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, New York

    Google Scholar 

  • Wyatt ASJ, Hewitt CL, Walker DI, Ward TJ (2005) Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment. Divers Distrib 11:33–44

    Article  Google Scholar 

  • Yamaguchi M (1975) Growth and reproductive cycles of marine fouling ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (Central Japan). Mar Biol 29:253–259

    Article  Google Scholar 

  • Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588

    Article  Google Scholar 

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Acknowledgments

We are grateful to J. Wong and J. Torkkola for help with collecting samples in the field. Also, thanks to S. FitzGibbon, S. O. Polsky and three anonymous reviewers for valuable comments. The research undertaken in this study was funded by Australian Greenhouse Office (AGO) and Australian Research Council (ARC). However, the views herein may not reflect those of the AGO or ARC.

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Correspondence to Gwendolyn K. David.

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Communicated by T. Reusch.

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David, G.K., Marshall, D.J. & Riginos, C. Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata . Mar Biol 157, 1955–1965 (2010). https://doi.org/10.1007/s00227-010-1464-y

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