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Population Structure of the SW Atlantic Estuarine Crab Neohelice granulata Throughout Its Range: a Genetic and Morphometric Study

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Abstract

Phylogeographic patterns of the SW Atlantic estuarine crab Neohelice granulata were examined using mitochondrial DNA cytochrome oxidase I sequences and analyzed together with morphometric data. Specimens were sampled during a 4-year period (2001–2004) from 11 localities encompassing the full distributional range of this species along the SW Atlantic (22°57′ S to 42°25′ S). DNA sequences were obtained from 69 individuals belonging to seven localities, and morphometric variation in 12 continuous characters was analyzed for 646 crabs from ten localities. Strong genetic differentiation, consistent with a pattern of isolation-by-distance, was detected among all localities indicating that gene flow occurs mainly between neighboring populations. Analyses of molecular variance showed genetic subdivision between the southern (Argentina) and the northern (Brazil) sites, suggesting restricted gene flow at a regional scale. The genetic structure of this species could be divided into two distinct groups due to a limited gene flow between southern and northern regions as a consequence of larval dispersal patterns. Coastal currents in the vicinity of the Rio de la Plata likely act as a barrier to dispersal within the species range. Moreover, genetic data indicate that populations of N. granulata might have undergone a northward demographic expansion since the late Pleistocene. The morphometric analysis showed no geographical pattern of morphological differentiation, although there were differences among sampling sites.

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References

  • Anastasiadou, C., and I.D. Leonardos. 2008. Morphological variation among populations of Atyaephyra desmarestii (Millet, 1831) (Decapoda: Caridea: Atyidae) from freshwater habitats of northwestern Greece. Journal of Crustacean Biology 28: 240–247.

    Article  Google Scholar 

  • Anger, K., C. Bas, E. Spivak, D. Ismael, and T. Luppi. 1994. Hatching rhythms and dispersion of decapod crustacean larvae in a brackish coastal lagoon in Argentina. Helgolander Meeresuntersuchungen 48: 445–466.

    Article  Google Scholar 

  • Anger, K., E. Spivak, T. Luppi, C. Bas, and D. Ismael. 2008. Larval salinity tolerance of the South American salt-marsh crab, Neohelice (Chasmagnathus) granulata: physiological constraints to estuarine retention, export and reimmigration. Helgoland Marine Research 62: 93–102.

    Article  Google Scholar 

  • Avise, J.C. 2004. Molecular markers, natural history and evolution. New York: Chapman and Hall.

    Google Scholar 

  • Balech, E., and M. Ehrlich. 2008. Esquema biogeográfico del mar Argentino. Revista de Investigación y Desarrollo Pesquero 19: 45–75.

    Google Scholar 

  • Bandelt, H.-J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  Google Scholar 

  • Bas, C., T. Luppi, and E. Spivak. 2005. Population structure of the South American estuarine crab, Chasmagnathus granulatus (Brachyura: Varunidae) near the southern limit of its geographical distribution: comparisons with northern populations. Hydrobiologia 537: 217–228.

    Article  Google Scholar 

  • Bas, C., T. Luppi, E. Spivak, and L. Schejter. 2009. Larval dispersion of the estuarine crab Neohelice granulata in coastal marine waters of the Southwest Atlantic. Estuarine, Coastal and Shelf Science 83: 569–576.

    Article  CAS  Google Scholar 

  • Becker, B.J., L.A. Levin, F.J. Fodrie, and P.A. McMillan. 2007. Complex larval connectivity patterns among marine invertebrate populations. Proceedings of the National Academy of Sciences of the United States of America 104: 3267–3272.

    Article  CAS  Google Scholar 

  • Bilton, D.T., J. Paula, and J.D.D. Bishop. 2002. Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science 55: 937–952.

    Article  Google Scholar 

  • Bogazzi, E., O. Iribarne, R. Guerrero, and E. Spivak. 2001. Exploring the causes of the southern limit of distribution of the SW Atlantic fiddler crab Uca uruguayensis. Journal of Shellfish Research 20: 353–360.

    Google Scholar 

  • Brian, J.V., T. Fernandes, R.J. Ladle, and P.A. Todd. 2006. Patterns of morphological and genetic variability in UK populations of the shore crab, Carcinus maenas Linnaeus, 1758 (Crustacea: Decapoda: Brachyura). Journal of Experimental Marine Biology and Ecology 329: 47–54.

    Article  Google Scholar 

  • Chenna, R., H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins, and J.D. Thompson. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

    Article  Google Scholar 

  • Couceiro, L., R. Barreiro, J.M. Ruiz, and E.E. Sotka. 2007. Genetic isolation by distance among populations of the netted dog whelk Nassarius reticulatus (L.) along the European Atlantic coastline. Journal of Heredity 98: 603–610.

    Article  CAS  Google Scholar 

  • Cowen, R.K., and S. Sponaugle. 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science 1: 443–466.

    Article  Google Scholar 

  • Cowen, R.K., C.B. Paris, and A. Srinivasan. 2006. Scaling of connectivity in marine populations. Science 311: 522–527.

    Article  CAS  Google Scholar 

  • Epifanio, C.E. 2007. Biology of larvae. In The blue crab Callinectes sapidus, ed. V.S. Kennedy and L.E. Cronin, 513–533. Maryland: Maryland Sea Grant College.

    Google Scholar 

  • Excoffier, L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lesson from the infinite-island model. Molecular Ecology 13: 853–864.

    Article  CAS  Google Scholar 

  • Excoffier, L., P.E. Smouse, and J.M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    CAS  Google Scholar 

  • Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.

    CAS  Google Scholar 

  • Favier Dubois, C.M., and F.L. Scartascini. 2012. Intensive fishery scenarios on the North Patagonian coast (Río Negro, Argentina) during the mid-Holocene. Quaternary International 256: 62–70.

    Article  Google Scholar 

  • Fernández Iriarte, P.J., M.P. Alonso, D.E. Sabadin, P.A. Arauz, and C.M. Iudica. 2011. Phylogeography of weakfish Cynoscion guatucupa (Perciformes: Sciaenidae) from the southwestern Atlantic. Scientia Marina 75: 701–706.

    Article  Google Scholar 

  • Forward, R.B., R.A. Tankersley, and J.M. Welch. 2003. Selective tidal-stream transport of the blue crab Callinectes sapidus: an overview. Bulletin of Marine Science 72: 347–365.

    Google Scholar 

  • Gebauer, P., I. Walter, and K. Anger. 1998. Effects of substratum and conspecific adults on the metamorphosis of Chasmagnathus granulata (Dana) (Decapoda: Grapsidae) megalopae. Journal of Experimental Marine Biology and Ecology 223: 185–198.

    Article  Google Scholar 

  • Giménez, L. 2003. Potential effects of physiological plastic responses to salinity on population networks of the estuarine crab Chasmagnathus granulata. Helgoland Marine Research 56: 265–273.

    Google Scholar 

  • Gopurenko, D., J.M. Hughes, and C.P. Keenan. 1999. Mitochondrial DNA evidence for rapid colonisation of the Indo-West Pacific by the mudcrab Scylla serrata. Marine Biology 134: 227–233.

    Article  Google Scholar 

  • Haig, J.A., R.M. Connolly, and J.M. Hughes. 2010. Little shrimp left on the shelf: the roles that sea-level change, ocean currents and continental shelf width play in the genetic connectivity of a seagrass-associated species. Journal of Biogeography 37: 1570–1583.

    Google Scholar 

  • Hellberg, M.E., R.S. Burton, J.E. Neigel, and S.R. Palumbi. 2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70: 273–290.

    Google Scholar 

  • Henzler, C.M., and A. Ingólfsson. 2007. The biogeography of the beachflea, Orchestia gammarellus (Crustacea, Amphipoda, Talitridae), in the North Atlantic with special reference to Iceland: a morphometric and genetic study. Zoologica Scripta 37: 57–70.

    Google Scholar 

  • Huret, M., I. Dadou, F. Dumas, P. Lazure, and V. Garçon. 2005. Coupling physical and biogeochemical processes in the Río de la Plata plume. Continental Shelf Research 25: 629–653.

    Article  Google Scholar 

  • Isacch, J.P., C.S.B. Costa, L. Rodríguez-Gallego, D. Conde, M. Escapa, D.A. Gagliardini, and O.O. Iribarne. 2006. Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient on the south-west Atlantic coast. Journal of Biogeography 33: 888–900.

    Article  Google Scholar 

  • Ituarte, R.B., E.D. Spivak, and T.A. Luppi. 2004. Female reproductive cycle of the Southwestern Atlantic estuarine crab Chasmagnathus granulatus (Brachyura: Grapsoidea: Varunidae). Scientia Marina 68: 127–137.

    Google Scholar 

  • Kawane, M., K. Wada, and K. Watanabe. 2008. Comparisons of genetic population structures in four intertidal brachyuran species of contrasting habitat characteristics. Marine Biology 156: 193–203.

    Article  Google Scholar 

  • Ketmaier, V., R. Argano, and A. Caccone. 2003. Phylogeography and molecular rates of subterranean aquatic stenasellid isopods with a peri-Tyrrhenian distribution. Molecular Ecology 12: 547–555.

    Article  CAS  Google Scholar 

  • Levin, L.A. 2006. Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46: 282–297.

    Article  CAS  Google Scholar 

  • Luppi, T., C. Bas, E. Spivak, and K. Anger. 1997. Fecundity of two grapsid crab species in the Laguna Mar Chiquita, Argentina. Archive of Fishery and Marine Research 45: 149–166.

    Google Scholar 

  • Luppi, T., E. Spivak, K. Anger, and J. Valero. 2002. Pattern and processes of Chasmagnathus granulata and Cyrtograpsus angulatus (Brachyura: Grapsidae) recruitment in Mar Chiquita Coastal Lagoon, Argentina. Estuarine, Coastal and Shelf Science 55: 287–297.

    Article  Google Scholar 

  • Luppi, T., C. Bas, and E. Spivak. 2003. The effect of temperature and salinity on larval development of Armases rubripes Rathbun, 1897 (Brachyura, Grapsoidea, Sesarmidae), and the southern limit of its geographical distribution. Estuarine, Coastal and Shelf Science 58: 575–585.

    Article  Google Scholar 

  • Luppi, T., C. Bas, A. Méndez Casariego, M. Albano, J. Lancia, M. Kittlein, A. Rosenthal, N. Farías, E. Spivak, and O. Iribarne. 2012. The influence of habitat, season and tidal regime in the activity of the intertidal crab Neohelice (=Chasmagnathus) granulata. Helgoland Marine Research. doi:10.1007/s10152-012-0300-9.

  • Manly, B.F.J. 1994. Multivariate statistical methods: a primer. Florida: Chapman and Hall.

    Google Scholar 

  • Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.

    CAS  Google Scholar 

  • Masci, K.D., M. Ponniah, and J.M. Hughes. 2008. Patterns of connectivity between the Lake Eyre and Gulf drainages, Australia: a phylogeographic approach. Marine and Freshwater Research 59: 751–760.

    Article  Google Scholar 

  • Miller, S.A., D.D. Dikes, and H.H. Polesky. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research 16: 215.

    Google Scholar 

  • Muelbert, J.H., M. Acha, H. Mianzán, R. Guerrero, R. Reta, E. Braga, V. Garcia, A. Berasategui, M. Gómez-Erache, and F. Ramírez. 2008. Biological, physical and chemical properties at the Subtropical Shelf front zone in the SW Atlantic continental shelf. Continental Shelf Research 28: 1662–1673.

    Article  Google Scholar 

  • Olsen, J.L., W.T. Stam, J.A. Coyer, T.B.H. Reusch, M. Billingham, C. Boström, E. Calvert, H. Christie, S. Granger, R. La Lumière, N. Milchakova, M.P. Oudot Le-Secq, G. Procaccini, B. Sanjabi, E. Serrão, J. Veldsink, S. Widdicombe, and S. Wyllie-Echeverria. 2004. North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Molecular Ecology 13: 1923–1941.

    Article  CAS  Google Scholar 

  • Palma, E.D., R.P. Matano, and A.R. Piola. 2004. A numerical study of the Southwestern Atlantic Shelf circulation: barotropic response to tidal and wind forcing. Journal of Geophysical Research 109: CO8014. doi:10.1029/2004JC002315.

    Article  Google Scholar 

  • Palma, E.D., R.P. Matano, and A.R. Piola. 2008. A numerical study of the Southwestern Atlantic Shelf circulation: stratified ocean response to local and offshore forcing. Journal of Geophysical Research 113: C11010. doi:10.1029/2007JC004720.

    Article  Google Scholar 

  • Piola, A.R., R.P. Matano, E.D. Palma, O.O. Möller, and E.J.D. Campos. 2005. The influence of the Plata River discharge on the western South Atlantic shelf. Geophysical Research Letters 32: LO1603. doi:10.1029/2004GL021638.

    Article  Google Scholar 

  • Piola, A.R., S.I. Romero, and U. Zajaczkovsky. 2008. Space-time variability of the Plata plume inferred from ocean color. Continental Shelf Research 28: 1556–1567.

    Article  Google Scholar 

  • Roehrdanz, R.L. 1993. An improved primer for PCR amplification of mitochondrial DNA in a variety of insect species. Insect Molecular Biology 2: 89–91.

    Article  CAS  Google Scholar 

  • Rozas, J., J.C. Sánchez-Delbarrio, X. Messeguer, and R. Rozas. 2003. DNASP4, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19: 2496–2497.

    Article  CAS  Google Scholar 

  • Scelzo, M.A. 2001. First record of the portunid crab Aranaeus cribarius (Lamarck, 1818) (Crustacea: Brachyura: Portunidae) in marine waters of Argentina. Proceedings of the Biological Society of Washington 114: 605–610.

    Google Scholar 

  • Schejter, L., E.D. Spivak, and T.A. Luppi. 2002. Presence of Pyromaia tuberculata (Lockington, 1877) adults and larvae in the Argentine continental shelf (Crustacea: Decapoda: Majoidea). Proceedings of the Biological Society of Washington 115: 605–610.

    Google Scholar 

  • Schneider, S., and L. Excoffier. 1999. Estimations of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152: 1079–1089.

    CAS  Google Scholar 

  • Siegel, D.A., S. Mitarai, C.J. Costello, S.D. Gaines, B.E. Kendall, R.R. Warner, and K.B. Winters. 2008. The stochastic nature of larval connectivity among nearshore marine populations. Proceedings of the National Academy of Sciences of the United States of America 105: 8974–8979.

    Article  CAS  Google Scholar 

  • Silva, I.C., N. Mesquita, and J. Paula. 2010. Lack of population structure in the fiddler crab Uca annulipes along an East African latitudinal gradient: genetic and morphometric evidence. Marine Biology 157: 1113–1126.

    Article  Google Scholar 

  • Simionato, C.G., V.L. Meccia, R. Guerrero, W.C. Dragani, and M. Nuñez. 2007. Rio de la Plata estuary response to wind variability in synoptic to intraseasonal scales: 2. Current´s vertical structure and its implications for the salt wedge structure. Journal of Geophysical Research 112: C07005. doi:10.1029/2006JC003815.

    Article  Google Scholar 

  • Slatkin, M. 1993. Isolation by distance in equilibrium and non equilibrium populations. Evolution 47: 264–279.

    Article  Google Scholar 

  • Spivak, E.D. 2010. The crab Neohelice (= Chasmagnathus) granulata: an emergent animal model from emergent countries. Helgoland Marine Research 64: 149–154.

    Article  Google Scholar 

  • Tankersley, R.A., M.G. Wieber, M.A. Sigala, and K.A. Kachurak. 1998. Migratory behavior of ovigerous blue crab Callinectes sapidus: evidence for selective tidal-stream transport. The Biological Bulletin 195: 168–173.

    Article  Google Scholar 

  • Valero, J., T. Luppi, and O. Iribarne. 1999. Size as indicator of swimming speed of crab megalopae. Journal of Shellfish Research 18: 663–666.

    Google Scholar 

  • Violante, R.A., and G. Parker. 2004. The post-glacial maximum transgression in the la Plata River and adjacent inner continental shelf, Argentina. Quaternary International 114: 167–181.

    Article  Google Scholar 

  • Von Zuben, F.J., L.C. Duarte, G. Stangenhaus, L.M. Pessoa, and S.F. dos Reis. 1998. Bootstrap confidence regions for canonical variates: application to studies of evolutionary differentiation. Biometrical Journal 40: 327–339.

    Article  Google Scholar 

  • Weersing, K., and R.J. Toonen. 2009. Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series 393: 1–12.

    Article  Google Scholar 

  • Wright, S. 1951. The genetical structure of populations. Annales Eugenics 15: 323–354.

    Article  Google Scholar 

  • Zar, J.H. 1999. Biostatistical analysis. New Jersey: Prentice Hall.

    Google Scholar 

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Acknowledgments

Financial support for this work came from Fundación Antorchas, Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). The Agencia Nacional de Investigación e Innovación (ANII) provided financial support to AD and EPL. We are grateful to Dr. Raul Reta, Dr. Marcelo Zarate, and Claudia Bas for helpful comments. RBI wishes to thank Ivanna Tomasco and Carolina Abud for their great help during lab training in molecular techniques. We also acknowledge two reviewers for constructive comments on an earlier version of this manuscript.

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Ituarte, R.B., D’Anatro, A., Luppi, T.A. et al. Population Structure of the SW Atlantic Estuarine Crab Neohelice granulata Throughout Its Range: a Genetic and Morphometric Study. Estuaries and Coasts 35, 1249–1260 (2012). https://doi.org/10.1007/s12237-012-9516-9

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