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Connectivity in solitary ascidians: Is a 24-h propagule duration sufficient to maintain large-scale genetic homogeneity?

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Abstract

Ascidians are considered to have lower dispersal potential than most other sessile marine invertebrates with planktonic propagules by virtue of a very brief propagule duration. The larvae of colonial forms remain in the water column for only a few minutes, whereas most solitary forms settle in less than 24 h. This difference in propagule duration has been used to explain why allozyme data from colonial ascidians on the Australian east coast were genetically distinct at different sampling sites, whereas a solitary species exhibited no genetic structure. Spatial homogeneity in solitary species is surprising because genetic structure of species with much higher dispersal potential can be characterised by isolation by geographic distance, suggesting that these disperse by means of a stepping-stone pattern of dispersal. I reassessed the dispersal potential of solitary ascidians using DNA sequence data from the mitochondrial cytochrome oxidase subunit 1 gene and the intron of the nuclear adenine nucleotide transporter gene of a common south-eastern Australian solitary ascidian, Pyura praeputialis, using samples that span the species’ distribution range. Congruent with earlier findings, there was no evidence for stepping-stone dispersal, but it must be conceded that these results could be strongly affected by frequent adult dispersal, particularly by means of anthropogenic vectors, as well as insufficient marker resolution.

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References

  • Ayre DJ, Davis AR, Billingham M, Llorens T, Styan C (1997) Genetic evidence for contrasting patterns of dispersal in solitary and colonial ascidians. Mar Biol 130:51–61

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  Google Scholar 

  • Bell JJ, Okamura B (2005) Low genetic diversity in marine nature reserve: re-evaluating diversity criteria in reserve design. Proc R Soc Lond B Biol Sci 272:1067–1074

    Article  CAS  Google Scholar 

  • Bentzen P (1998) Seeking evidence of local stock structure using molecular genetic methods. In: Hunt von Herbing I, Kornfield I, Tupper M, Wilson J (eds) The implications of localized fishery stocks. Regional Agricultural Engineering Service, New York, pp 20–30

    Google Scholar 

  • Bingham RL, Young CM (1991) Larval behaviour 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 

  • Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrel fishes (family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913

    Article  Google Scholar 

  • Castilla JC, Manríquez PH, Delgado AP, Gargallo L, Leiva A, Radic D (2007) Bio-foam enhances larval retention in a free-spawning marine tunicate. Proc Natl Acad Sci USA 104:18120–18122

    Article  CAS  Google Scholar 

  • Clark M, Ortiz V, Castilla JC (1999) Does early development of the Chilean tunicate Pyura praeputialis (Heller, 1878) explain the restricted distribution of the species? Bull Mar Sci 65:745–754

    Google Scholar 

  • Coleman MA, Roughan M, Macdonald HS, Connell SD, Gillanders BM, Kelaher BP, Steinberg PD (2011) Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. J Ecol 99:1026–1032

    Article  Google Scholar 

  • Crandall EC, Treml EA, Barber PH (2012) Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Mol Ecol 21:5579–5598

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Grosberg RK (1991) Sperm-mediated gene flow and the genetic structure of a population of the colonial sea squirt Botryllus schlosseri. Evolution 45:130–142

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148

    Google Scholar 

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

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  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 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  Google Scholar 

  • Petersen JK, Svane I (1995) Larval dispersal in the ascidian Ciona intestinalis (L.). Evidence for a closed population. J Exp Mar Biol Ecol 186:89–102

    Article  Google Scholar 

  • Pogson GH, Taggart CT, Mesa KA, Boutilier RG (2001) Isolation by distance in the Atlantic cod, Gadus morhua, at large and small geographic scales. Evolution 55:131–146

    Article  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Rius M, Teske PR (2011) A revision of the Pyura stolonifera species complex (Tunicata, Ascidiacea), with a description of a new species from Australia. Zootaxa 2754:27–40

    Google Scholar 

  • Rius M, Teske PR (2013) Cryptic diversity in coastal Australasia: a morphological and mito-nuclear genetic analysis of habitat-forming sibling species. Zool J Linn Soc 168:597–611

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stephens M, Donelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  Google Scholar 

  • Stephens M, Smith N, Donelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  Google Scholar 

  • Stobutzki IC (2000) Marine reserves and the complexity of larval dispersal. Rev Fish Biol Fisheries 10:515–518

    Article  Google Scholar 

  • Sunnucks P, Hale DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  Google Scholar 

  • Teske PR, Papadopoulos I, Zardi GI, McQuaid CD, Edkins MT, Griffiths CL, Barker NP (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152:697–711

    Article  Google Scholar 

  • Teske PR, Rius M, McQuaid CD, Styan CA, Piggott MP, Benhissoune S, Fuentes-Grunewald C, Walls K, Page M, Attard CRM, Cooke GM, McClusky CF, Banks SC, Barker NP, Beheregaray LB (2011) “Nested” cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions. BMC Evol Biol 11:176

    Article  Google Scholar 

  • van Duyl FC, Bak RPM, Sybesma J (1981) The ecology of the tropical compound ascidian Tridemnum solidum. I. Reproductive strategy and larval behaviour. Mar Ecol Prog Ser 6:35–42

    Article  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 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Worcester SE (1994) Adult rafting versus larval swimming: dispersal and recruitment of a botryllid ascidian on eelgrass. Mar Biol 121:309–317

    Article  Google Scholar 

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Acknowledgments

I am grateful to Jonathan Sandoval-Castillo and Tess Cole for helping with the sampling. This research was supported by the University of Johannesburg.

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  1. Department of Zoology, University of Johannesburg, Auckland Park 2006, Johannesburg, South Africa

    Peter R. Teske

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  1. Peter R. Teske
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Correspondence to Peter R. Teske.

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Communicated by C. Riginos.

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Teske, P.R. Connectivity in solitary ascidians: Is a 24-h propagule duration sufficient to maintain large-scale genetic homogeneity?. Mar Biol 161, 2681–2687 (2014). https://doi.org/10.1007/s00227-014-2522-7

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