Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T06:05:40.533Z Has data issue: false hasContentIssue false
  • English
  • Français

Distinctness, phylogenetic relations and biogeography of intertidal mussels (Brachidontes, Mytilidae) from the south-western Atlantic

Published online by Cambridge University Press:  03 May 2013

Berenice Trovant ,
Daniel E. Ruzzante ,
Néstor G. Basso  and
J.M. (Lobo) Orensanz
Berenice Trovant*
Affiliation:
Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina
Daniel E. Ruzzante
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
Néstor G. Basso
Affiliation:
Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina
J.M. (Lobo) Orensanz
Affiliation:
Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina
*
Correspondence should be addressed to: B. Trovant, Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina email: trovant@cenpat.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

Rocky shore intertidal communities along the cold- and warm-temperate coasts of the south-western Atlantic are dominated by small mussels of the genus Brachidontes s.l. (Mytilidae), yet the status of species occurring in the region remains unresolved. Taxonomic studies have been based on shell morphology, but high phenotypic variability has led to much confusion. Based on mitochondrial and nuclear genes (COI, 28S rDNA and ITS1) from nine localities in Uruguay and Argentina we confirmed the occurrence of three species in the south-western Atlantic: Brachidontes darwinianus and B. rodriguezii in the warm-temperate and B. purpuratus in the cold-temperate sector. The latter two species coexist in the same beds along the transition zone (41–43°S). The phylogeny based on mitochondrial and nuclear genes, indicate an early divergence of B. purpuratus. At the intra-specific level, low genetic differentiation and absence of fossil record for B. purpuratus from the earlier Quaternary marine terraces of Patagonia likely result from a relatively recent (post-LGM) colonization originated from populations in the south-eastern Pacific. In the case of B. rodriguezii, by contrast, genetic intraspecific differentiation, a fossil record of phenotypically-related forms going back to the Late Miocene, and phylogenetic position in the COI-based phylogeny, prompts the hypothesis that this species is derived from a local stock with a long history of occurrence in the warm-temperate region of the south-western Atlantic. While intertidal mussel beds from the south-western Atlantic are ecologically similar in appearance, their assembly involves components clearly differentiated in terms of historical biogeography and phylogeny.

Keywords

BrachidontesmusselCOI barcodingnuclear DNAphylogenysouth-western Atlantic
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 7 , November 2013 , pp. 1843 - 1855
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adami, M.L., Pastorino, G. and Orensanz, J.M. (2013) Phenotypic differentiation of ecologically-significant Brachidontes species co-occurring in intertidal mussel beds from the southwestern Atlantic. Malacologia 56.CrossRefGoogle Scholar
Aguirre, M.L. (1994) Type specimens of Quaternary marine bivalves from Argentina. Ameghiniana 31, 347–374.Google Scholar
Aguirre, M.L., Perez, S.I. and Negro-Sirch, Y. (2006a) Morphological variability of Brachidontes Swainson (Bivalvia, Mytilidae) in the marine Quaternary of Argentina (SW Atlantic). Palaeogeography, Palaeoclimatology, Palaeoecology 239, 100–125.CrossRefGoogle Scholar
Aguirre, M.L., Richiano, S. and Negro-Sirch, Y. (2006b) Palaeoenvironments and palaeoclimates of the Quaternary molluscan faunas from the coastal area of Bahia Vera-Camarones (Chubut, Patagonia). Palaeogeography, Palaeoclimatology, Palaeoecology 229, 251–286.CrossRefGoogle Scholar
Aguirre, M.L., Hlebszevitsch-Savalscky, J.C. and Dellatorre, F. (2008) Late Cenozoic invertebrate paleontology of Patagonia and Tierra del Fuego, with emphasis on molluscs. In Rabassa, J. (ed.) The Late Cenozoic of Patagonia and Tierra del Fuego. Amsterdam: Elsevier, pp. 285–324.CrossRefGoogle Scholar
Avelar, W.E.P. and Narchi, W. (1983) Behavioral aspects of Brachidontes darwinianus darwinianus (Orbigny, 1846) and Brachidontes solisianus (Orbigny, 1846) (Bivalvia, Mytilidae) in response to a salinity gradient. Iheringia (Zool) 63, 125–132.Google Scholar
Balech, E. and Ehrlich, M.D. (2008) Esquema Biogeográfico del Mar Argentino. Revista de Investigación y Desarrollo Pesquero 19, 45–75.Google Scholar
Ballard, J.W.O. and Whitlock, M.C. (2004) The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.CrossRefGoogle ScholarPubMed
Bandelt, H.J., Forster, P.I. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Briggs, J.C. and Bowen, B.W. (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography 39, 12–30.CrossRefGoogle Scholar
Bucklin, A., Steinke, D. and Blanco-Bercial, L. (2011) DNA Barcoding of marine metazoa. Annual Review of Marine Science 3, 471–508.CrossRefGoogle ScholarPubMed
Ceballos, S.G., Lessa, E.P., Victorio, M.F. and Fernández, D.A. (2012) Phylogeography of the sub-Antarctic notothenioid fish Eleginops maclovinus: evidence of population expansion. Marine Biology 159, 499–505.CrossRefGoogle Scholar
Coan, E.V. and Valentich-Scott, P. (2012) Bivalve seashells of tropical West America. Marine bivalve mollusks from Baja, California to Northern Peru. Santa Barbara, CA: Santa Barbara Museum.Google Scholar
de Aranzamendi, M.C., Bastida, R. and Gardenal, C.N. (2011) Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Marine Biology 158, 2405–2418.CrossRefGoogle Scholar
del Río, C. and Martínez, S.A. (1998) Moluscos marinos miocenos de la Argentina y del Uruguay. Monografías de la Academia Nacional de Ciencias Exactas, Físicas y Naturales 15, 95 pp.Google Scholar
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. and Robledo, C.W. (2011) InfoStat. Grupo InfoStat FCA, Universidad Nacional de Córdoba, Argentina.Google Scholar
Distel, D.L. (2000) Phylogenetic relationships among Mytilidae (Bivalvia): 18S rRNA data suggest convergence in mytilid body plans. Molecular Phylogenetics and Evolution 15, 25–33.CrossRefGoogle ScholarPubMed
d'Orbigny, A. (1842) Mollusques. Voyage dans l'Amérique Méridionale 5. Paris: P. Bertrand, pp. 83–85.Google Scholar
d'Orbigny, A. (1846) Mollusques. Voyage dans l'Amérique Méridionale 5. Paris: P. Bertrand, pp. 489–758.Google Scholar
Excoffier, L. and Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology and Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Excoffier, L., Smouse, P.E. and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Farris, J.S., Källersjö, M., Kluge, A.G. and Bult, C. (1995) Testing significance of congruence. Cladistics 10, 315–319.CrossRefGoogle Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Fernández, M., Jaramillo, E., Marquet, P.A., Moreno, C.A., Navarrete, S.A., Ojeda, F.P., Valdovinos, C.R. and Vásquez, J.A. (2000) Diversity, dynamics and biogeography of Chilean benthic nearshore ecosystems: an overview and guidelines for conservation. Revista Chilena de Historia Natural 73, 797–830.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fraser, C.I., Thiel, M., Spencer, H.G. and Waters, J.M. (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. Evolutionary Biology 10, 203.Google ScholarPubMed
Fraser, C.I., Nikula, R., Ruzzante, D.E. and Waters, J.M. (2012) Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends in Ecology and Evolution 27, 462–471.CrossRefGoogle ScholarPubMed
Funk, D.J. and Omland, K.E. (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34, 397–423.CrossRefGoogle Scholar
Garrido-Ramos, M.A., Stewart, D.T., Sutherland, B.W. and Zouros, E. (1998) The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: implications for the operation of doubly uniparental inheritance of mitochondrial DNA. Genome 41, 818–824.CrossRefGoogle Scholar
González-Wevar, C.A., Nakano, T., Cañete, J.I. and Poulin, E. (2011) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Molecular Ecology 20, 1936–1951.CrossRefGoogle ScholarPubMed
Goto, T.V., Tamate, H.B. and Hanzawa, N. (2011) Phylogenetic characterization of three morphs of mussels (Bivalvia, Mytilidae) inhabiting isolated marine environments in Palau Islands. Zoological Science 28, 568–579.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. and deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B—Biological Sciences 270, 313–322.CrossRefGoogle ScholarPubMed
Huber, M. (2010) Compendium of bivalves. A full-color guide to 3300 of the world's marine bivalves. A status on Bivalvia after 250 years of research. Hackenheim: ConchBooks.Google Scholar
Huson, D.H., Richter, D.C., Rausch, C., Dezulian, T., Franz, M. and Rupp, R. (2007) Dendroscope: an interactive viewer for large phylogenetic trees. Bioinformatics 8, 460.Google ScholarPubMed
Kelaher, B.P., Castilla, J.C., Prado, L., York, P., Schwindt, E. and Bortolus, A. (2007) Spatial variation in molluscan assemblages from coralline turfs of Argentinean Patagonia. Journal of Molluscan Studies 73, 139–146.CrossRefGoogle Scholar
Kyriakou, E., Zouros, E. and Rodakis, G.C. (2010) The atypical presence of the paternal mitochondrial DNA in somatic tissues of male and female individuals of the blue mussel species Mytilus galloprovincialis. BMC Research Notes 3, 222.CrossRefGoogle ScholarPubMed
Lee, T. and Ó Foighil, D. (2004) Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complex. Molecular Ecology 13, 3527–3542.CrossRefGoogle ScholarPubMed
Lee, T. and Ó Foighil, D. (2005) Placing the floridian marine genetic disjunction into regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex. Evolution 59, 39–58.Google ScholarPubMed
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefGoogle ScholarPubMed
Liuzzi, M.G. and López Gappa, J. (2008) Macrofaunal assemblages associated with coralline turf: species turnover and changes in structure at different spatial scales. Marine Ecology Progress Series 363, 147–156.CrossRefGoogle Scholar
Macaya, E.C. and Zuccarello, G.C. (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Marine Ecology Progress Series 420, 103–112.CrossRefGoogle Scholar
Matsumoto, M. (2003) Phylogenetic analysis of the subclass Pteriomorphia (Bivalvia) from mtDNA COI sequences. Molecular Phylogenetics and Evolution 27, 429–440.CrossRefGoogle ScholarPubMed
Melvill, J.C. and Standen, R. (1914) Notes on Mollusca collected in the North-west Falklands by Mr Rupert Vallentin FLS, with descriptions of six new species. Annual Magazine of Natural History 13, 110–137.CrossRefGoogle Scholar
Mouquet, N., Devictor, V., Meynard, C.N., Munoz, F., Bersier, L.F., Chave, J., Couteron, P., Dalecky, A., Fontaine, C., Gravel, D., Hardy, O.J., Jabot, F., Lavergne, S., Leibold, M., Mouillot, D., Münkemüller, T., Pavoine, S., Prinzing, A., Rodrigues, A.S.L., Rohr, R.P., Thébault, E. and Thuiller, W. (2012) Ecophylogenetics: advances and perspectives. Biological Reviews 87, 769–785.CrossRefGoogle ScholarPubMed
Nixon, K.C. and Wheeler, Q.D. (1990) An amplification of the phylogenetic species concept. Cladistics 621, 1–223.Google Scholar
Olsson, A.A. (1961) Mollusks of the tropical eastern Pacific. Panamic–Pacific Pelecypoda. Ithaca, NY: Paleontological Research Institution.Google Scholar
Owada, M. and Hoeksema, B.W. (2011) Molecular phylogeny and shell microstructure of Fungiacava eilatensis Goreau et al. 1968, boring into mushroom corals (Scleractinia: Fungiidae), in relation to other mussels (Bivalvia: Mytilidae). Contributions to Zoology 80, 169–178.CrossRefGoogle Scholar
Park, J. and Ó Foighil, D. (2000) Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments. Molecular Phylogenetics and Evolution 14, 75–88.CrossRefGoogle ScholarPubMed
Parks, D.H., Porter, M., Churcher, S., Wang, S., Blouin, C., Whalley, J., Brooks, S. and Beiko, R.G. (2009) GenGIS: a geospatial information system for genomic data. Genome Research 19, 1896–1904.CrossRefGoogle ScholarPubMed
Pérez, M., Guiñez, R., Llanova, A., Toro, J.E., Astorga, M. and Presa, P. (2008) Development of microsatellite markers for the ecosystem bioengineer mussel Perumytilus purpuratus and cross-priming testing in six Mytilinae genera. Molecular Ecology Resources 8, 449–451.CrossRefGoogle ScholarPubMed
Pérez-García, C., Cambeiro, J.M., Morán, P. and Pasantes, J.J. (2010a) Chromosomal mapping of rDNAs, core histone genes and telomeric sequences in Perumytilus purpuratus (Bivalvia: Mytilidae). Journal of Experimental Marine Biology and Ecology 395, 199–205.CrossRefGoogle Scholar
Pérez-García, C., Guerra-Varela, J., Morán, P. and Pasantes, J.J. (2010b) Chromosomal mapping of rRNA genes, core histone genes and telomeric sequences in Brachidontes puniceus and Brachidontes rodriguezi (Bivalvia, Mytilidae). BMC Genetics 11, 1–8.CrossRefGoogle ScholarPubMed
Polzin, T. and Daneschmand, S.V. (2003) On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters 31, 12–20.CrossRefGoogle Scholar
Ponce, J.F., Rabassa, J., Coronato, A. and Borromei, A.M. (2011) Palaeogeographical evolution of the Atlantic coast of Pampa and Patagonia from the last glacial maximum to the Middle Holocene. Biological Journal of the Linnean Society 103, 363–379.CrossRefGoogle Scholar
Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Rabassa, J., Coronato, A. and Martínez, O. (2011) Late Cenozoic glaciations in Patagonia and Tierra del Fuego: an updated review. Biological Journal of the Linnean Society 103, 316–335.CrossRefGoogle Scholar
Rawson, P.D. and Hilbish, T.J. (1995) Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Molecular Biology and Evolution 12, 893–901.Google ScholarPubMed
Richards, H.G. and Craig, J.R. (1963) Pleistocene sedimentation and fauna of the Argentine shelf. II. Pleistocene mollusks from the continental shelf of Argentina. Proceedings of the Academy of Natural Sciences of Philadelphia 115, 113–152.Google Scholar
Ríos, C., Mutschke, E. and Morrison, E. (2003) Benthic sublitoral biodiversity in the Strait of Magellan, Chile. Revista de Biología Marina y Oceanografía 38, 1–12.Google Scholar
Rios, E.C. (1994) Seashells of Brazil. Rio Grande do Sul: Museu Oceanográfico da FURG.Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. BMC Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Ruzzante, D.E., Walde, S.J., Gosse, J.C., Cussac, V.E., Habit, E., Zemlak, T.S. and Adams, E.D.M. (2008) Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography. Molecular Ecology 17, 2234–2244.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning. A laboratory manual. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Scarabino, F. (2003) Lista sistemática de los Bivalvia marinos y estuarinos vivientes de Uruguay. Comunicaciones de la Sociedad Malacológica del Uruguay 8, 229–259.Google Scholar
Scarabino, F., Zaffaroni, J.C., Clavijo, C., Carranza, A. and Nin, M. (2006) Bivalvos marinos y estuarinos de la costa uruguaya: faunística, distribución, taxonomía y conservación. In Menafra, R., Rodríguez-Gallego, L., Scarabino, F. and Conde, D. (eds) Bases para la Conservación y el Manejo de la Costa Uruguaya. Montevideo: Vida Silvestre Publicaciones, pp. 157–170.Google Scholar
Scarabino, V. (1977) Moluscos del Golfo San Matías (Prov. De Río Negro, Rep. Argentina). Comunicaciones de la Sociedad Malacológica del Uruguay 4, 177–286.Google Scholar
SEGEMAR (Servicio Geológico Minero Argentino) (2000) Mapa geológico de la República Argentina, escala 1:2.500.000. Buenos Aires: Instituto de Geología y Recursos Naturales.Google Scholar
Silliman, B.R., Bertness, M.D., Altieri, A.H., Griffin, J.N., Bazterrica, M.C., Hidalgo, F.J., Crain, C.M. and Reyna, M.V. (2011) Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS ONE 6, e24502. doi:24510.21371/journal.pone.0024502CrossRefGoogle ScholarPubMed
Skibinski, D.O.F., Gallagher, C. and Beynon, C.M. (1994) Mitochondrial DNA inheritance. Nature 368, 817–818.CrossRefGoogle ScholarPubMed
Swofford, D.L. (1998) PAUP*. Phylogenetic analysis using Parsimony (*and other methods). Sunderland, MA: Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA 4: Molecular Evolutionary Genetics Analysis. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Tanaka, M.O. and Magalhães, C.A. (2002) Edge effects and succession dynamics in Brachidontes mussel beds. Marine Ecology Progress Series 237, 151–158.CrossRefGoogle Scholar
Terranova, M.S., Lo Brutto, S., Arculeo, M. and Mitton, J.B. (2007) A mitochondrial phylogeography of Brachidontes variabilis (Bivalvia: Mytilidae) reveals three cryptic species. Journal of Zoological Systematics and Evolutionary Research 45, 289–298.CrossRefGoogle Scholar
Thiel, M. and Ullrich, N. (2002) Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgoland Marine Research 56, 21–30.CrossRefGoogle Scholar
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
van der Molen, S., Márquez, F., Idaszkin, Y.L. and Adami, M. (2012) Use of shell-shape to discriminate between Brachidontes rodriguezii and Brachidontes purpuratus species (Mytilidae) in the transition zone of their distributions (south-western Atlantic). Journal of the Marine Biological Association of the United Kingdom, doi: http://dx.doi.org/10.1017/S0025315412001221Google Scholar
Waters, J.M., Fraser, C.I. and Hewitt, G.M. (2012) Founder takes all: density-dependent processes structure biodiversity. Trends in Ecology and Evolution 28, 78–85.CrossRefGoogle ScholarPubMed
Webb, C.O., Ackerly, D.D., McPeek, M.A. and Donoghue, M.J. (2002) Phylogenies and community ecology. Annual Review of Ecology, Evolution, and Systematics 33, 475–505.CrossRefGoogle Scholar
White, L.R., McPherson, B.A. and Stauffer, J.R. (1996) Molecular genetic identification tools for the unionids of French Creek, Pennsylvania. Malacologia 38, 181–202.Google Scholar
WoRMS (World Registry of Marine Species) (2013) Available at: http://www.marinespecies.org (accessed 25 March 2013).Google Scholar
Zelaya, D.G. (2009) Bivalvia. In Häussermann, V. and Försterra, G. (eds) Marine benthic fauna of Chilean Patagonia. Puerto Montt: Nature in Focus, pp. 426–454.Google Scholar
Zouros, E., Freeman, K.R., Ball, A.O. and Pogson, G.H. (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359, 412–414.CrossRefGoogle ScholarPubMed
Supplementary material: File

Trovant Supplementary Material

Appendix

Download Trovant Supplementary Material(File)
File 215 KB