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Marine Biology

, Volume 162, Issue 3, pp 595–605 | Cite as

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

  • J. D. NuñezEmail author
  • P. J. Fernández Iriarte
  • E. H. Ocampo
  • C. Iudica
  • M. Cledón
Original Paper

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.

Keywords

Haplotype Network Genetic Diversity Index Pelagic Larval Duration Atlantic Population Pacific Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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).

References

  1. 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 285–325Google Scholar
  2. Aguirre ML, Richiano S, Álvarez MF, Eastoe C (2009) Malacofauna Cuaternaria del litoral norte de Santa Cruz (Patagonia, Argentina). Geobios 42:411–434CrossRefGoogle Scholar
  3. Alamo V, Valdivieso V (1997) Lista sistemática de moluscos marinos del Perú. Segunda edición, revisada y actualizada, Instituto del Mar del Perú, CallaoGoogle Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University, CambridgeGoogle Scholar
  5. Becker BJ, Levin LA, Fodrie FJ, McMillan PA (2007) Complex larval connectivity patterns among marine invertebrate populations. Proc Natl Acad Sci USA 104:3267–3272CrossRefGoogle Scholar
  6. 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 103:630–637CrossRefGoogle Scholar
  7. 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 36:969–981CrossRefGoogle Scholar
  8. 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–S107CrossRefGoogle Scholar
  9. 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 PlataGoogle Scholar
  10. Ceballos SG, Lessa EP, Victorio MF, Fernández DA (2012) Phylogeography of the sub-Antarctic notothenioid fish Eleginops maclovinus: evidence of population expansion. Mar Biol 159:499–505CrossRefGoogle Scholar
  11. 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 158:2405–2418CrossRefGoogle Scholar
  12. Dell RK (1971) The marine mollusca of the Royal Society Expedition to Southern Chile, 1958–59. Records of the Dominion Museum 7: 155–233Google Scholar
  13. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  14. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192CrossRefGoogle Scholar
  15. Emerson BC, Hewitt GM (2005) Phylogeography. Curr Biol 15:367–371CrossRefGoogle Scholar
  16. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0. An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  18. 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 75:701–706CrossRefGoogle Scholar
  19. Filatov DA (2002) ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624CrossRefGoogle Scholar
  20. 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 3:294–299Google Scholar
  21. 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 106:3249–3253CrossRefGoogle Scholar
  22. 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 10:203CrossRefGoogle Scholar
  23. Fraser CI, Nikula R, Ruzzante DE, Waters JW (2012) Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends Ecol Evol 27:462–471CrossRefGoogle Scholar
  24. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  25. 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 20:1936–1951CrossRefGoogle Scholar
  26. 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 12:139CrossRefGoogle Scholar
  27. 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 22:5221–5236CrossRefGoogle Scholar
  28. 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 88:673–689CrossRefGoogle Scholar
  29. Harrison S (2004) The Pleistocene glaciations of Chile. In: Ehlers J, Gibbard PL (eds) Quaternary glaciations: extent and chronology, vol 3. Elsevier, BostonGoogle Scholar
  30. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  31. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  32. Hewitt GM (2001) Speciation, hybrid zones, and phylogeography: seeing genes in space and time. Mol Ecol 10:537–549CrossRefGoogle Scholar
  33. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans Biol Sci 359:183–195CrossRefGoogle Scholar
  34. 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 271–294Google Scholar
  35. 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 104:2785–2790CrossRefGoogle Scholar
  36. 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 22:1561–1568CrossRefGoogle Scholar
  37. Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56:517–522CrossRefGoogle Scholar
  38. Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101CrossRefGoogle Scholar
  39. Hulton NRJ, Purves RS, McCulloch RD, Sugden DE, Bentley MJ (2002) The last glacial maximum and deglaciation in southern South America. Quat Sci Rev 21:233–241CrossRefGoogle Scholar
  40. 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 7:220CrossRefGoogle Scholar
  41. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  42. Librado P, Rozas J (2009) DNAsp v. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  43. Macaya EC, Zuccarello GC (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112CrossRefGoogle Scholar
  44. 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 19:146–169CrossRefGoogle Scholar
  45. 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 15:409–417CrossRefGoogle Scholar
  46. 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 14:203–212CrossRefGoogle Scholar
  47. 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 65:347–359CrossRefGoogle Scholar
  48. 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 169:27–42CrossRefGoogle Scholar
  49. 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 9:469–491Google Scholar
  50. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  51. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158CrossRefGoogle Scholar
  52. 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 ArgentinoGoogle Scholar
  53. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  54. Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571CrossRefGoogle Scholar
  55. 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 20:81–103CrossRefGoogle Scholar
  56. Rabassa J, Coronato A, Martínez O (2011) Late Cenozoic glaciations in Patagonia and Tierra del Fuego: an updated review. Biol J Linn Soc 103:316–335CrossRefGoogle Scholar
  57. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefGoogle Scholar
  58. 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 34:566–575CrossRefGoogle Scholar
  59. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  60. 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 15:2949–2968CrossRefGoogle Scholar
  61. 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 103:475–494CrossRefGoogle Scholar
  62. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68CrossRefGoogle Scholar
  63. 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 95:106–116CrossRefGoogle Scholar
  64. Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601Google Scholar
  65. 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 28:2731–2739CrossRefGoogle Scholar
  66. 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 20:5025–5041CrossRefGoogle Scholar
  67. 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 70:291–308Google Scholar
  68. 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 138:831–841CrossRefGoogle Scholar
  69. 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 10:506–513Google Scholar
  70. Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Mol Ecol 11:1131–1144CrossRefGoogle Scholar
  71. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469CrossRefGoogle Scholar
  72. 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 394:165–177CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • J. D. Nuñez
    • 1
    Email author
  • P. J. Fernández Iriarte
    • 1
  • E. H. Ocampo
    • 1
  • C. Iudica
    • 1
  • M. Cledón
    • 1
  1. 1.IIMyC, Instituto de Investigaciones Marinas y Costeras, CONICET – FCEyNUniversidad Nacional de Mar del PlataMar del PlataArgentina

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