Abstract
The phylogeography of two sympatric Magellanic limpets of the genus Nacella was studied. The historical and contemporary processes underlying their intraspecific patterns in Argentina were inferred using the mitochondrial cytochrome oxidase I gene. Results indicate different evolutionary histories in the two species. A recent geographic and demographic expansion ~11,000 years ago, with absence of current genetic structuring, is proposed for Nacella magellanica. In contrast, the phylogeographic pattern showed noticeable phylogenetic and geographic discontinuities in Nacella deaurata; slow continuous population size growth with current low levels of gene flow among its populations was also observed, indicating demographic equilibrium. The beginning of divergence between these closely related limpets was estimated at about 270,000 years ago with very little or none gene flow occurring after their splitting. These contrasting historic patterns could be related to distinctive responses to climate changes associated with Pleistocene glaciations, as a result of differences in their ecological traits.
Similar content being viewed by others
References
Aguirre ML, Negro Sirch Y, Richiano S (2005) Late Quaternary molluscan assemblages from the coastal area of Bahía Bustamante (Patagonia, Argentina): paleoecology and paleoenviroments. J S Am Earth Sci 20:13–32
Aguirre ML, Richiano S, Álvarez MF, Eastoe C (2009) Malacofauna Cuaternaria del litoral norte de Santa Cruz (Patagonia, Argentina). Geobios 42:411–434
Avise JC (2000) Phylogeography, the history and formation of species. Harvard University Press. Cambridge, Massachusetts, USA
Avise JC (2004) Molecular markers, natural history, and evolution. Sinauer Associates. Inc, Massachusetts, USA
Becker BJ, Levin LA, Fodrie FJ, McMillan PA (2007) Complex larval connectivity patterns among marine invertebrate populations. Proc Natl Acad Sci USA 104(9):3267–3272
Berthier P, Excoffier L, Ruedi M (2006) Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc R Soc B 273:3101–3109
Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186
Bird C, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141
Bowden DA, Clarke A, Peck LS, Barnes DKA (2006) Antarctic sessile marine benthos: colonisation and growth on artificial substrata over three years. Mar Ecol Prog Ser 316:1–16
Carcelles A (1947) Sobre algunas especies del género Nacella Schumacher. Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo, II Nº 40
Carcelles A (1959) Catálogo de los Moluscos Marinos de la Patagonia. Anales del Museo Nahuel, Huapi. I. Buenos Aires
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Colgan DJ, Schreiter S (2011) Extrinsic and intrinsic influences on the phylogeography of the Austrocochlea constricta species group. J Exp Mar Biol Ecol 397:44–51
Collin R (2001) The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Mol Ecol 10:2249–2262
Coronato A, Meglioli A, Rabassa J (2004) Glaciations in the Magellan Straits and Tierra del Fuego, Southernmost South America. In: Ehlers J, Gibbard P (eds) Quaternary Glaciations - Extent and Chronology. Quaternary Book Series, Part III. Elsevier Publishers, pp 45–48
Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626
Cuevas JM, Martin JP, Bastida R (2006) Benthic community changes in a patagonian intertidal: a forty years later comparison. Thalassas 22(1):31–39. ISSN: 0212-5919
de Aranzamendi MC, Sahade R, Tatián M, Chiappero MB (2008) Genetic differentiation between morphotypes in the Antarctic limpet Nacella concinna as revealed by Inter-simple Sequence Repeat markers. Mar Biol 154:875–885
de Aranzamendi MC, Gardenal CN, Martin JP, Bastida R (2009) Limpets of the genus Nacella (Mollusca, Gastropoda) from the southwestern Atlantic coast: species identification based on molecular data. J Molluscan Stud 75:241–251
de Castellanos ZJA, Landoni N (1988) Catálogo descriptivo de la malacofauna marina magallánica. 2 Archigastropoda: Scissurellidae, Patellidae, Acmaeidae y Lepetidae. Fissurellidae, Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC)
Deng QE, Hazel W (2010) Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California. Mar Biol 157:1989–2000
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22(5):1185–1192
Edgar R (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. Bioinformatics 5:113–131. http://www.drive5.com/muscle
Excoffier L, Schneider S (1999) Why hunter-gathered populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online
Folmer O, Black M, Heah 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
García-Moreno J, Arctander P, Fjeldså J (1999) A case of rapid diversification in the neotropics: phylogenetic relationships among Cranioleuca Spinetails (Aves, Furnariidae). Mol Phylogenet Evol 12(3):273–281
Gmelin JF (1791) Systema naturae per regna tria naturae. In: Linneaeus, C. 13th edn. Leipzig, Vol. 1, Part 6 (Vermes), pp 3021–3910
Goldson AJ, Hughes RN, Gliddon CJ (2001) Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans. Mar Biol 138(5):1037–1042
Goldstien SJ, Schiel DR, Gemmell NJ (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268
González-Wevar CA, Nakano T, Canete JI, Poulin E (2010) Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean. Mol Phylogenet Evol 56:115–124
González-Wevar CA, David B, Poulin E (2011a) Phylogeography and demographic inference in Nacella (Patinigera) concinna (Strebel, 1908) in the western Antarctic Peninsula. Deep-Sea Res Part II: Top Stud Oceanogr 58:220–229
González-Wevar CA, Nakano T, Canete JI, Poulin E (2011b) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Mol Ecol 20(9):1936–1951
Gordillo S (1999) Holocene molluscan assemblages in the Magellan region. Sci Mar 63(1):15–22
Gordillo S, Coronato A, Rabassa J (2005) Quaternary molluscan faunas from the island of Tierra del Fuego after the Last Glacial Maximum. Sci Mar 69(2):337–348
Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Heusser CJ (1989) Late Quaternary vegetation and climate of southern Tierra del Fuego. Quatern Res 31:396–406
Heusser CJ (1998) Deglacial paleoclimate of the American sector of the Southern Ocean: late Glacial-Holocene records from the latitude of Canal Beagle (55°S), Argentine Tierra del Fuego. Palaeogeogr Palaeoclimateol Palaeoecol 141:277–301
Hey J (2005) On the number of new world founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3:0965–0975
Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760
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
Ho SYW, Shapiro B, Phyllips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of Molecular Rate Estimates. Syst Biol 56:517–522
Hoffman JI, Peck LS, Linse K, Clarke A (2010) Strong population genetic structure in a broadcast-spawning Antarctic marine invertebrate. J Heredity 154:765–778
Kemppainen P, Panova M, Hollander J, Johannesson K (2009) Complete lack of mitochondrial divergence between two species of NE Atlantic marine intertidal gastropods. J Evol Biol 22:2000–2011
Kindal BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environmentals: a community perspective. Ecology 84(8):2007–2020
Kirkendale LA, Meyer CP (2004) Phylogeography of the Patelloida profunda group (Gastropoda: Lottidae): diversification in a dispersal‐driven marine system. Mol Ecol 13:2749–2762
Malanga G, Estevez MS, Calvo J, Puntarulo S (2004) Oxidative stress in limpets exposed to different environment conditions in the Beagle Channel. Aquat Toxicol 69:299–309
Malanga G, Estevez MS, Calvo J, Abele D, Puntarulo S (2007) The effect of seasonality on oxidative metabolism in Nacella (Patinigera) magellanica. Comp Biochem Physiol A 146:551–558
Maniatis T, Fritsh EF, Sambrook J (1982) Molecular cloning. A laboratory manual, Cold Spring Harbor Laboratory. Cold Spring Harbor, New York
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
McCarthy C (1998) Chromas ver. 1.45. School of Health Science, Griffith University, Queensland, Australia. http://www.technelysium.com.au/chromas.html
McCulloch R, Bentley M (1998) Late glacial ice advances in the Strait of Magellan, southern Chile. Quaternary Science Reviews 17:775–787
Morriconi E (1999) Reproductive biology of the limpet Nacella (P.) deaurata (Gmelin, 1791 in Bahía Lapataia (Beagle Channel). Sci Mar 63(1):417–426
Morriconi E, Calvo J (1993) Environmental influence on shell allometric growth in Nacella (Patinigera) deaurata (Gmelin 1791) from the Beagle Channel, Argentina. Malacologia 35(1):135–140
Muellner AN, Tremetsberger K, Stuessy T, Baeza CM (2005) Pleistocene refugia and recolonization routes in the southern Andes: insights from Hypochaeris palustris (Asteraceae, Lactuceae). Mol Ecol 14:203–212
Murray-Jones SE, Ayre DJ (1997) High levels of gene flow in the surf bivalve Donax deltoids (Bivalvia: Donacidae) on the east coast of Australia. Mar Biol 128:83–89
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, USA
Olivier S, Paternoster IJ, Bastida R (1966) Estudios Biocenóticos en las costas del Chubut (Argentina). I. Zonación Biológica de Puerto Pardelas (Golfo Nuevo). Boletín del Instituto de Biología Marina 10:1–74
Otaegui AV (1974) Las especies del género Patinigera Dall, 1905 en la Provincia Magallánica (Mollusca, Gastropoda, Prosobranchiata). Physis Secc B 33(86):173–184
Pannacciulli FG, Manetti G, Maltagliati F (2009) Genetic diversity in two barnacle species, Chthamalus stellatus and Tesseropora atlantica (Crustacea, Cirripedia), with different larval dispersal modes in the archipelago of the Azores. Mar Biol 156(12):2441–2450
Paulay G, Meyer C (2006) Dispersal and divergence across the greatest ocean region: do larvae matter? Integr Comp Biol 46(3):269–281
Pilsbry HA (1891) Manual of conchology 13. Academy of Natural Sciences. Philadelphia, Pennsilvania, USA
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Powell AWB (1973) The patellid limpets of the world (Patellidae). Indo-Pacific Mollusca 3:75–206
Rabassa J, Bujalesky G, Gordillo S, Roig C, Salemme M (1992) The Quaternary of Tierra del Fuego: the status of knowledge. Sveriges Geologiska Undersökning ser. Ca. 81:249–256
Rabassa J, Coronato A, Salemme M (2005) Chronology of the Late Cenozoic Patagonian Glaciations and their correlation with biostratigraphic units of the Pampean Region (Argentina). J South Am Earth Sci 20:81–103
Rambaut A, Drummond AJ (2007) Tracer v1.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, Scotland. http://tree.bio.ed.ac.uk
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Real LE, Julio N, Gardenal NC, Ciocco NF (2004) Genetic variability of Tehuelche scallop, Aequipecten tehuelchus, populations from the Patagonian coasts (Argentina). J Mar Biol Ass UK 84:235–238
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Ruzzante DE, Walde SJ, Cussac VE, Dalebout ML, Seibert J, Ortubay S, Habit E (2006) Phylogeography of the Percichthyidae (Pisces) in Patagonia: roles of orogeny, glaciation, and volcanism. Mol Ecol 15:2949–2968
Ruzzante DE, Walde SJ, Gosse JC, Cussac VE, Habit E, Zemlak TS, Adams EDM (2008) Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography. Mol Ecol 17:2234–2244
Sá-Pinto A, Branco M, Sayanda D, Alexandrino P (2008) Patterns of colonization, evolution and gene flow in specie of the genus Patella in the Macaronesian Islands. Mol Ecol 17:519–532
Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68
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(1):106–116
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562
Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integ Comp Biol 42:780–789
Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
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
Valdovinos C, Rüth M (2005) Nacellidae limpets of the southern end of South America: taxonomy and distribution. Rev Chil Hist Nat 78:497–517
Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55(12):2455–2469
Weihe E, Kriews M, Abele D (2010) Differences in heavy metal concentrations and in the response of the antioxidant system to hypoxia and air exposure in the Antarctic limpet Nacella concinna. Mar Environ Res 69:127–135
Won YJ, Hey J (2005) Divergence population genetics of chimpanzees. Mol Biol Evol 22:297–307
Acknowledgments
We are grateful to Alvina Lèche, Juan José Martínez and Guillermo Albrieu for their support and their useful comments on the manuscript. We thank Raúl González-Ittig and Marina Chiappero for guidance with computer programs, and J. P. Martin, A. Argüeso, M. Turic, M. Narvarte and M. Gavensky who helped in collecting part of the sampling. MCdA is a Postdoctoral Fellow and RB and CNG are Career Investigators of the CONICET.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Riginos.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Aranzamendi, M.C., Bastida, R. & Gardenal, C.N. Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Mar Biol 158, 2405–2418 (2011). https://doi.org/10.1007/s00227-011-1742-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1742-3