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Deep phylogeographic divergence among populations of limpet Siphonaria lessoni on the east and west coasts of South America

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Abstract

The historical processes that have influenced the genetic structure of many species are often associated with environmental changes of the Pleistocene glacial cycles. These climate changes involve temperature oscillation, marine currents and loss of coastal habitats, which could have affected the abundance and geographic distribution of marine species in temperate coastal habitats. In this work, a 552-bp mtDNA fragment of COI locus of 92 individuals was sequenced to analyze the genetic structure of the limpet Siphonaria lessoni. Individuals were collected on the intertidal coast of the Southern Atlantic (Mar del Plata, San Antonio Oeste, Puerto Madryn and Ushuaia in Argentina) and the Southern Pacific (Valdivia and Valparaíso in Chile). S. lessoni displayed two distinct lineages that were nearly reciprocally monophyletic between the Atlantic and Pacific coasts. AMOVA tests revealed the existence of strong population genetic structure. The Pacific coasts yielded more haplotypes and polymorphic sites as well as higher haplotype and nucleotide diversity than the Atlantic clade did. Both Tajima’s D and Fu’s F s were significant and negative, suggesting that limpet populations are in population expansion or have recently expanded. Accordingly, the haplotype network for each clade showed a star-like phylogeographic pattern. From IMa analysis, the divergence time between Pacific and Atlantic populations was 100,000–1,000,000 ybp with gene flow occurring from Pacific to Atlantic populations. The Bayesian Skyline analysis revealed an older coalescence in the Pacific clade (30,000–300,000 ybp) as compared to that in the Atlantic clade (4,000–40,000 ybp). This work reports evidence of Pacific–Atlantic geographic isolation with asymmetric migration, which is probably related to changes in sea level and temperature due to the extended glaciation periods that occurred in the region throughout the Pleistocene.

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References

  • Aguirre ML, Hlebzsebitch J, Dellatorre F (2008) Late Cenozoic Invertebrate Paleontology, with emphasis on Mollusks. In: Rabassa, J. (ed), The Late Cenozoic of Patagonia and Tierra del Fuego. Chapter 14. Developments in Quaternary Sciences, 11, Elsevier, Amsterdam, p 285–325

  • Aguirre ML, Richiano S, Álvarez MF, Eastoe C (2009) Malacofauna Cuaternaria del litoral norte de Santa Cruz (Patagonia, Argentina). Geobios 42:411–434

    Article  Google Scholar 

  • Alamo V, Valdivieso V (1997) Lista sistemática de moluscos marinos del Perú. Segunda edición, revisada y actualizada, Instituto del Mar del Perú, Callao

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University, Cambridge

    Google Scholar 

  • Becker BJ, Levin LA, Fodrie FJ, McMillan PA (2007) Complex larval connectivity patterns among marine invertebrate populations. Proc Natl Acad Sci USA 104:3267–3272

    Article  CAS  Google Scholar 

  • Brante A, Fernández M, Viard F (2012) Phylogeography and biogeography concordance in the marine gastropod Crepipatella dilatata (Calyptraeidae) along the southeastern Pacific coast. J Hered 103:630–637

    Article  Google Scholar 

  • Cárdenas L, Castilla JC, Viard F (2009) A phylogeographical analysis across three biogeographical provinces of the south-eastern Pacific: the case of the marine gastropod Concholepas concholepas. J Biogeogr 36:969–981

    Article  Google Scholar 

  • Carr MH, Neigel JE, Estes JA, Andelman S, Warner RR, Largier JL (2003) Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecol Appl 13:S90–S107

    Article  Google Scholar 

  • Castellanos ZJA, Landoni NA, Dadon JR (1993) Opistobranchia excepto Nudibranchida, y Pulmonata. Catálogo descriptivo de la malacofauna marina magallánica. 12. Comisión de Investigaciones Científicas Provincia de Buenos Aires, La Plata

  • Ceballos SG, Lessa EP, Victorio MF, Fernández DA (2012) Phylogeography of the sub-Antarctic notothenioid fish Eleginops maclovinus: evidence of population expansion. Mar Biol 159:499–505

    Article  Google Scholar 

  • de Aranzamendi MC, Bastida R, Gardenal CN (2011) Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the south-western Atlantic coast. Mar Biol 158:2405–2418

    Article  Google Scholar 

  • Dell RK (1971) The marine mollusca of the Royal Society Expedition to Southern Chile, 1958–59. Records of the Dominion Museum 7: 155–233

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  CAS  Google Scholar 

  • Emerson BC, Hewitt GM (2005) Phylogeography. Curr Biol 15:367–371

    Article  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 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernández Iriarte P, Alonso MP, Sabadin D, Arauz PA, Iudica C (2011) Phylogeography of weakfish Cynoscion guatucupa (Perciformes: Sciaenidae) from the southwestern Atlantic. Sci Mar 75:701–706

    Article  Google Scholar 

  • Filatov DA (2002) ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624

    Article  CAS  Google Scholar 

  • 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 Biotech 3:294–299

    CAS  Google Scholar 

  • Fraser CI, Nikula R, Spencer HG, Waters JM (2009) Kelp genes reveal effects of subantarctic sea ice during the last glacial maximum. Proc Natl Acad Sci USA 106:3249–3253

    Article  CAS  Google Scholar 

  • Fraser CI, Thiel M, Spencer H, Waters J (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evol Biol 10:203

    Article  Google Scholar 

  • Fraser CI, Nikula R, Ruzzante DE, Waters JW (2012) Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends Ecol Evol 27:462–471

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  Google Scholar 

  • González-Wevar CA, Nakano T, Cañete JI, Poulin E (2011) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic province. Mol Ecol 20:1936–1951

    Article  Google Scholar 

  • González-Wevar CA, Hüne M, Cañete JI, Mansilla A, Nakano T, Poulin E (2012) Towards a model of postglacial biogeography in shallow marine species along the Patagonian province: lessons from the limpet Nacella magellanica (Gmelin, 1791). BMC Evol Biol 12:139

    Article  Google Scholar 

  • González-Wevar CA, Saucède T, Morley SA, Chown SL, Poulin E (2013) Extinction and recolonization of maritime Antarctica in the limpet Nacella concinna (Strebel, 1908) during the last glacial cycle: toward a model of Quaternary biogeography in shallow Antarctic invertebrates. Mol Ecol 22:5221–5236

    Article  Google Scholar 

  • Grant WS, Bowen BW (2006) Living in a tilted world: climate change and geography limit speciation in Old World anchovies (Engraulis; Engraulidae). Biol J Linn Soc 88:673–689

    Article  Google Scholar 

  • Harrison S (2004) The Pleistocene glaciations of Chile. In: Ehlers J, Gibbard PL (eds) Quaternary glaciations: extent and chronology, vol 3. Elsevier, Boston

    Google Scholar 

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  Google Scholar 

  • Hewitt GM (2001) Speciation, hybrid zones, and phylogeography: seeing genes in space and time. Mol Ecol 10:537–549

    Article  CAS  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans Biol Sci 359:183–195

    Article  CAS  Google Scholar 

  • Hewitt GM, Ibrahim KM (2001) Inferring glacial refugia and historical migrations with molecular phylogenies. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. BES symposium volume. Blackwell Press, Oxford, pp 271–294

    Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790

    Article  CAS  Google Scholar 

  • Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimated and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568

    Article  CAS  Google Scholar 

  • Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56:517–522

    Article  Google Scholar 

  • Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101

    Article  Google Scholar 

  • Hulton NRJ, Purves RS, McCulloch RD, Sugden DE, Bentley MJ (2002) The last glacial maximum and deglaciation in southern South America. Quat Sci Rev 21:233–241

    Article  Google Scholar 

  • Janko K, Lecointre G, DeVries A, Couloux A, Cruaud C, Marshall C (2007) Did glacial advances during the Pleistocene influence differently the demographic histories of benthic and pelagic Antarctic shelf fishes? Inferences from intraspecific mitochondrial and nuclear DNA sequence diversity. BMC Evol Biol 7:220

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DNAsp v. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • Macaya EC, Zuccarello GC (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112

    Article  Google Scholar 

  • Marko PB, Hoffman JM, Emme SA, McGovern TM, Keever CC, Cox LN (2010) The ‘Expansion–Contraction’ model of Pleistocene biogeography: rocky shores suffer a sea change? Mol Ecol 19:146–169

    Article  CAS  Google Scholar 

  • McCulloch RD, Bentley MJ, Purves RS, Hulton NRJ, Sugden DE, Clapperton CM (2000) Climatic inferences from glacial and palaeoecological evidence at the last glacial termination, southern South America. J Quat Sci 15:409–417

    Article  Google Scholar 

  • Muellner A, Tremetsberger K, Stuessy T, Baeza C (2005) Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae). Mol Ecol 14:203–212

    Article  CAS  Google Scholar 

  • Ocampo EH, Nuñez JD, Lizarralde MS, Cledón M (2011) Larval development of Calyptraeotheres garthi (Fenucci, 1975) (Brachyura, Pinnotheridae) described from laboratory reared material, with notes of larval character use on Pinnotheridae systematic. Helgol Mar Res 65:347–359

    Article  Google Scholar 

  • Ocampo EH, Robles R, Terossi M, Nuñez JD, Cledón M, Mantelatto FL (2013) Phylogeny, phylogeography, and systematics of the American pea crab genus Calyptraeotheres Campos, 1990, inferred from molecular markers. Zool J Linn Soc Lond 169:27–42

    Article  Google Scholar 

  • Olivier SR, Penchaszadeh PE (1968) Observaciones sobre la ecología y biología de Siphonaria (Pachysiphonaria) lessoni (Blainivlle, 1824) (Gastropoda, Siphonariidae) en el litoral rocoso de Mar del Plata (Buenos Aires). Cah Biol Mar 9:469–491

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158

    Article  Google Scholar 

  • Penchaszadeh P, Pastorino G, Brögger M (2007) Moluscos gasterópodos y bivalvos: Siphonaria lessoni. En: Boltovskoy D (ed). Atlas de sensibilidad ambiental de la costa y el Mar Argentino

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571

    Article  Google Scholar 

  • Rabassa J, Coronato AM, Salemme M (2005) Chronology of the Late Cenozoic Patagonian glaciations and their correlation with biostratigraphic units of the Pampean region (Argentina). J S Am Earth Sci 20:81–103

    Article  Google Scholar 

  • Rabassa J, Coronato A, Martínez O (2011) Late Cenozoic glaciations in Patagonia and Tierra del Fuego: an updated review. Biol J Linn Soc 103:316–335

    Article  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    Article  CAS  Google Scholar 

  • Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  Google Scholar 

  • Ruzzante D, Walde S, Cussac V, Dalebout M, Seibert J, Ortubay S, Habit E (2006) Phylogeography of the Percichthyidae (Pisces) in Patagonia: roles of orogeny, glaciations, and volcanism. Mol Ecol 15:2949–2968

    Article  CAS  Google Scholar 

  • Sérsic AN, Cosacov A, Cocucc IAA, Johnson LA, Pozner R, Avila LJ, Sites JW Jr, Morando M (2011) Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biol J Linn Soc 103:475–494

    Article  Google Scholar 

  • Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68

    Article  Google Scholar 

  • Sherman CDH, Hunt A, Ayre DJ (2008) Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol J Linn Soc 95:106–116

    Article  Google Scholar 

  • Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Teske PR, Papadopoulos I, Mmonwa KL, Matumba TG, McQuaid CD, Barker NP, Beheregaray LB (2011) Climate-driven genetic divergence of limpets with different life histories across a southeast African marine biogeographic disjunction: different processes, same outcome. Mol Ecol 20:5025–5041

    Article  Google Scholar 

  • Thorrold SR, Jones GP, Hellberg ME, Burton RS, Swearer SE, Neigel JE, Morgan SG, Warner RR (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull Mar Sci 70:291–308

    Google Scholar 

  • Túnez JI, Cappozzo HL, Nardelli M, Cassini MH (2010) Population genetic structure and historical population dynamics of the South American sea lion, Otaria flavescens, in north-central Patagonia. Genetica 138:831–841

    Article  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  Google Scholar 

  • Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Mol Ecol 11:1131–1144

    Article  CAS  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469

    Article  CAS  Google Scholar 

  • Zakas C, Binford J, Navarrete SA, Wares JP (2009) Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone. Mar Ecol Prog Ser 394:165–177

    Article  Google Scholar 

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Acknowledgements

This work was supported by the following grants: PIP 2504 (2009–2011) and PIP 798 (2012–2014) (CONICET) 15/E534 and 15/E627 (UNMdP) awarded to P.F.I. Additional support for J.D.N. and E.H.O. was provided by a PhD scholarship funded by CONICET. Authors wish explicitly to thank reviewers’ and editor’ comments for having largely improved this article. They are also grateful to M.P. Oteiza for the manuscript revision and helpful advice. Authors would also like to thank D. Sabadin, P. Lertora, N. Chiaradia, C. Matula and M.R Garcia-Huidobro Moreno for assistance during field work. The present results are part of the PhD thesis of J.D.N., P.F.I. and M.C., who are members of the Scientific Researcher Program of CONICET (Argentina).

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  1. IIMyC, Instituto de Investigaciones Marinas y Costeras, CONICET – FCEyN, Universidad Nacional de Mar del Plata, Funes 3250 (7600), Mar del Plata, Provincia de Buenos Aires, Argentina

    J. D. Nuñez, P. J. Fernández Iriarte, E. H. Ocampo, C. Iudica & M. Cledón

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  1. J. D. Nuñez
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  2. P. J. Fernández Iriarte
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  3. E. H. Ocampo
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Correspondence to J. D. Nuñez.

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Communicated by C. Riginos.

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Nuñez, J.D., Fernández Iriarte, P.J., Ocampo, E.H. et al. Deep phylogeographic divergence among populations of limpet Siphonaria lessoni on the east and west coasts of South America. Mar Biol 162, 595–605 (2015). https://doi.org/10.1007/s00227-014-2607-3

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