Abstract
In Antarctica, ascidians are among the most conspicuous and abundant organisms in benthic ecosystems and many species present wide distribution patterns. Two similar forms of ascidians of the colonial genus Synoicum were sampled along the South Shetland Islands, one greenish-yellow with elongated colony stalks and the other yellow-orange with shorter stalks and more rounded colony bodies. The taxonomic analyses indicated that the greenish-yellow form corresponded to the description of the species S. ostentor and the yellow-orange form to that of S. adareanum. However, molecular analyses using the cytochrome oxidase I gene did not detect clear differences between both forms. The frequency and geographic distribution of haplotypes indicate that some degree of gene flow may be occurring, strongly suggesting that both morphotypes did not achieve a complete reproductive isolation yet, that they can still interbreed and should therefore be considered as a single species. Surprisingly, these results are not in line with recent studies of Antarctic fauna using a similar approach, which revealed several cases of morphologically indistinguishable but genetically distinct species.
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References
Allcock AL, Strugnell JM (2012) Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol Evol 27:520–528
Allcock AL, Barratt I, Eléaume M, Linse K, Norman MD, Smith PJ, Steinke D, Stevens DW, Strugnell JM (2011) Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Res II 58:242–249
Baird HP, Miller KJ, Stark JS (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol Ecol 20:3439–3454
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Barnes DKA, Hodgson DA, Convey P, Allen CS, Clarke A (2006) Incursion and excursion of Antarctic biota: past, present and future. Global Ecol Biogeogr 15:121–142
Bernardi G, Goswami U (1997) Molecular evidence for cryptic species among the Antarctic fish Trematomus bernacchii and Trematomus hansoni. Antarct Sci 9:381–385
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155
Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Single-locus and multilocus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. Oxford University Press, Oxford, pp 225–269
Clarke A (1996) The distribution of Antarctic marine benthic communities. In: Hofmann EE, Ross RM, Quetin LB (eds) Foundations for ecological research west of the Antarctic Peninsula. Antarct Res Ser, AGU, Washington, DC, pp 219–230
Clarke A, Crame JA (1989) The origin of the southern ocean marine fauna. In: Crame JA (ed) Origins and evolution of the Antarctic Biota. The Geological Society, London, pp 253–268
Clarke A, Johnston NM (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol 41:47–114
Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3
Dayton PK (1990) Polar benthos. In: Smith W (ed) Polar oceanography. Academic Press, New York, pp 631–685
Demarchi M, Chiappero MB, Tatián M, Sahade R (2010) Population genetic structure of the Antarctic ascidian Aplidium falklandicum from Scotia Arc and South Shetland Islands. Polar Biol 33:1567–1576
Diyabalange T, Amsler CD, McClintock JB, Baker BJ (2006) Palmerolide A, a Cytotoxic Macrolide from the Antarctic Tunicate Synoicum adareanum. J Am Chem Soc 128:5630–5631
Dowdeswell JA, Bamber JL (2007) Keel depths of modern Antarctic icebergs and implications for sea-floor scouring in the geological record. Mar Geol 243:120–131
Excoffier L, Schneider S (1999) Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602
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
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501
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
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gili JM, Arntz WE, Palanques A, Orejas C, Clarke A, Dayton PK, Isla E, Teixidó N, Rossi S, López-González PJ (2006) A unique assemblage of epibenthic sessile suspension feeders with archaic features in the high-Antarctic. Deep-Sea Res II 53:1029–1052
Goldstien SJ, Schiel DR, Gemmell NJ (2010) Regional connectivity and coastal expansion: differentiating pre-border and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885
Goodall-Copestake WP, Tarling GA, Murphy EJ (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56
Grosberg RK, Cunningham CW (2001) Genetic structure in the sea from populations to communities. In: Bertness MD, Hay ME, Gaines SD (eds) Marine community ecology. Sinauer, Sunderland, MA, pp 61–84
Gutt J (2000) Some “driving forces” structuring communities of the sublittoral Antarctic macrobenthos. Antarct Sci 12:297–313
Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Haydar D, Hoarau G, Olsen JL, Stam WT, Wolff WJ (2011) Introduced or glacial relict? Phylogeography of the cryptogenic tunicate Molgula manhattensis (Ascidiacea, Pleurogona). Divers Distrib 17:68–80
Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes AH, Gieskes WW, Rozema J, Schorno RM, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 135–139
Herdman WA (1902) Tunicata. In: Report on the collections of natural history made in the Antarctic regions during the voyage of the “Southern Cross”, London, pp 190–200
Hirose E, Oka AT, Hirose M (2009) Two new species of photosymbiotic ascidians of the genus Diplosoma from the Ryukyu Archipelago, with partial sequences of the COI gene. Zool Sci 26:362–368
Hirose M, Nozawa Y, Hirose E (2010) Genetic isolation among Morphotypes in the Photosymbiotic Didemnid Didemnum molle (Ascidiacea, Tunicata) from the Ryukyus and Taiwan. Zool Sci 27:959–964
Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the Drake Passage in the Southern Ocean. J Hered 99:137–148
Jiang X, Liu B, Lebreton S, De Brabander JK (2007) Total synthesis and structure revision of the marine metabolite Palmerolide A. J Am Chem Soc 129:6386–6387
Koplovitz G, McClintock JB, Amsler CD, Baker BJ (2011) A comprehensive evaluation of the potential chemical defenses of Antarctic ascidians against sympatric fouling microorganisms. Mar Biol 158:2661–2671
Kott P (1969) Antarctic Ascidiacea. Antarctic Res Ser 13:1–239
Lawver LA, Gahagan LM, Dalziel IWD (2011) A different look at gateways: Drake Passage and Australia/Antarctica. In: Anderson JB, Wellner JS (eds) Tectonic, climatic, and cryospheric evolution of the Antarctic Peninsula. AGU, Washington, DC, pp 5–33
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
López-Legentil S, Turon X (2005) How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Polycitoridae). Zool Scr 34:3–14
López-Legentil S, Turon X (2006) Population genetics, phylogeography and speciation of Cystodytes (Ascidiacea) in the western Mediterranean Sea. Biol J Linn Soc 88:203–214
López-Legentil S, Dieckmann R, Bontemps-Subielos N, Turon X, Banaigs B (2005) Qualitative variation of alkaloids in color morphs of Cystodytes (Ascidiacea). Biochem Syst Ecol 33:1107–1119
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
Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394
Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587
McCarthy C (1998) Chromas ver. 1.45. School of Health Science, Griffith University, Queensland, Australia. http://www.technelysium.com.au/chromas.html. Accessed 14 Dec 2012
Millar RH (1960) Ascidiacea. Discov Rep 30:1–160
Monniot C, Monniot F (1983) Ascidies antarctiques et sub-antarctiques: morphologie et biogéographie. Mem Mus Nat Hist Nat Nouv Ser A 125:1–168
Monniot F, Dettai A, Eleaume M, Cruaud C, Ameziane N (2011) Antarctic Ascidians (Tunicata) of the French-Australian survey CEAMARC in Terre Adélie. Zootaxa 2817:1–54
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nicolaou KC, Guduru R, Sun Y-P, Banerji B, Chen DY-K (2007) Total synthesis of the originally proposed and revised structures of Palmerolide A. Angew Chem Int Ed 46:5896–5900
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572
Pérez-Portela R, Turon X (2008) Phylogenetic relationships of the Clavelinidae and Pycnoclavellidae (Ascidiacea) inferred from mtDNA data. Invertebr Biol 127:108–120
Pérez-Portela R, Duran S, Palacín C, Turon X (2007) The genus Pycnoclavella (Ascidiacea) in the Atlanto-Mediterranean region: a combined molecular and morphological approach. Invertebr Syst 21:187–205
Pineda MC, López-Legentil S, Turon X (2011) The Whereabouts of an Ancient Wanderer: global Phylogeography of the Solitary Ascidian Styela plicata. PlosONE 6:e25495
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Raupach MJ, Wägele JW (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)—a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191–198
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
Riesenfeld CS, Murray AE, Baker BJ (2008) Characterization of the microbial community and Polyketide biosynthetic potential in the Palmerolide-producing tunicate Synoicum adareanum. J Nat Prod 71:1812–1818
Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Phil Trans R Soc B 362:2191–2214
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Ronquist F, Huelsenbeck J (2003) Mrbayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sabbadin A (1982) Formal genetics of ascidians. Am Zool 22:765–773
Savidge DK, Amft JA (2009) Circulation on the West Antarctic Peninsula derived from 6 years of shipboard ADCP transects. Deep-Sea Res I 56:1633–1655
Stoner DS, Weissman IL (1996) Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. Evolution 93:15254–15259
Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90
Swofford DL (2001) PAUP: phylogenetic analysis using parsimony (and other methods) Version 4. Sinauer Associates, Sunderland, MA
Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Mar Biol 130:455–462
Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2004) Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Mol Ecol 13:3125–3136
Thatje S (2012) Effects of capability for dispersal on the evolution of diversity in antarctic benthos. Integr Comp Biol 52:470–482
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882
Turon X, Tarjuelo I, Duran S, Pascual M (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503:29–35
Van Name WG (1945) The North and South American ascidians. Bull Am Mus Nat Hist 84:1–476
Wares JP, Gaines SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55:295–306
Wright S (1969) Evolution and the genetics of populations. The theory of gene frequencies, vol 2. University of Chicago Press, Chicago, IL
Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588
Acknowledgments
We thank the crew and participants of the BENTART-06 (BIO Hespérides) for their help and assistance and Ana Ramos for her support. We are grateful to Milagros Demarchi and Cristian Lagger who helped in collecting part of the samples. Financial and logistic supports were provided by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto Antártico Argentino (IAA), Fondo para la Investigación Científica y Tecnológica (FONCyT) and the National University of Córdoba.
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Wiernes, M.P., Sahade, R., Tatián, M. et al. Genetic variability and differentiation among polymorphic populations of the genus Synoicum (Tunicata, Ascidiacea) from the South Shetland Islands. Polar Biol 36, 871–883 (2013). https://doi.org/10.1007/s00300-013-1312-x
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DOI: https://doi.org/10.1007/s00300-013-1312-x