Scientia Marina, Vol 74, No 3 (2010)

Population differentiation of the shore crab Carcinus maenas (Brachyura: Portunidae) on the southwest English coast based on genetic and morphometric analyses


https://doi.org/10.3989/scimar.2010.74n3435

Inês C. Silva
Centro de Oceanografia, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa - The Marine Biological Association of the UK , United Kingdom

M. Judite Alves
Museu Nacional de História Natural, Universidade de Lisboa - Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa , Portugal

Jose Paula
Centro de Oceanografia, Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa , Portugal

Stephen J. Hawkins
The Marine Biological Association of the UK - School of Ocean Sciences, University of Wales Bangor , United Kingdom

Abstract


Carcinus maenas has a planktonic larval phase which can potentially disperse over large distances. Consequently, larval transport is expected to play an important role in promoting gene flow and determining population structure. In the present study, population structuring on the southwest coast of England was analysed using molecular and morphometric approaches. Variation at eight microsatellite loci suggested that the individuals sampled within this region comprise a single genetic population and that gene flow among them is not restricted. Nevertheless, the FST values estimated across loci for all populations suggested that the Tamar population was significantly different from the Exe, Camel and Torridge populations. This differentiation is not explained by isolation by distance, and coastal hydrological events that are apparently influencing larval flux might be the cause of this pattern. Morphometric analysis was also performed. Analysis of carapace and chela shape variation using landmark-based geometric morphometrics revealed extensive morphological variability, as the multivariate analysis of variance showed significant morphometric differences among geographic groups for both sexes. Thus, the morphological differentiation found may be a plastic response to habitat-specific selection pressures.

Keywords


Carcinus maenas; microsatellites; population structure; geometric morphometrics; phenotypic plasticity; gene flow

Full Text:


PDF

References


Bagley, M.J. and J.B. Geller. – 1999. Microsatellite DNA analysis of native and invading populations of European Green crabs. Proc. Natl, Conf. Mar. Bioinvasions. MIT Sea Grant Publication, Cambridge (MA).

Baldridge, A.K. and L.D. Smith. – 2008. Temperature constraints on phenotypic plasticity explain biogeographic patterns in predator trophic morphology. Mar. Ecol. Prog. Ser., 365: 25-34. doi:10.3354/meps07485

Bilton, D.T., J. Paula and J.D.D. Bishop. – 2002. Dispersal, genetic differentiation and speciation in estuarine organisms. Est. Coast. Shelf Sci., 55: 937-952. doi:10.1006/ecss.2002.1037

Bollens, S.M., B.W. Frost, D. S. Thoreson and S.J. Watts. – 1992. Diel vertical migration in zooplankton: field evidence in support of the predator avoidance hypothesis. Hydrobiologia, 234: 33-39.

Brian, J.V. – 2005. Inter-population variability in the reproductive morphology of the shore crab (Carcinus maenas): evidence of endocrine disruption in a marine crustacean? Mar. Pollut. Bull., 50: 410-416. doi:10.1016/j.marpolbul.2004.11.023 PMid:15823302

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). J. Exp. Mar. Biol. Ecol., 329: 47-54. doi:10.1016/j.jembe.2005.08.002

Brookfield, J.F.Y. -1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol., 5: 453-455. PMid:8688964

Bulnheim, H.-P. and S. Bahns. – 1996. Genetic variation and divergence in the Genus Carcinus (Crustacea, Decapoda).Int. Rev. Gesamten Hydrobiol., 81: 611-619.

Cavalcanti, M.J. – 2005. Mantel for Windows version 1.18.

Corander, J., P. Marttinen and S. Mäntyniemi. – 2005. Bayesian identification of stock mixtures from molecular marker data. Fish. Bull., 104: 550-558.

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. PMid:1644282    PMCid:1205020

Excoffier, L., G. Laval and S. Schneider. – 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinformatics Online, 1: 47-50. PMid:19325852    PMCid:2658868

Goudet, J. – 1999. PCA-GEN for Windows. Version 1.2.

Goudet, J. – 2002. FSTAT: a program to estimate and test gene diversities and fixation indices. Version 2.9.3.2.

Hillis, D.M., B.K. Mable, A. Larson, S.K. Davis and E.A. Zimmer. – 1996. Nucleic Acids IV: Sequencing and cloning. In: D.M. Hillis, C. Moritz and B.K. Mable (eds), Molecular Systematics (2nd ed.), Sinauer Associates Inc., Sunderland (MA).

Hollander, J., M L. Collyer, D.C. Adams and K. Johannesson. – 2006. Phenotypic plasticity in two marine snails: constraints superseding life history. J. Evol. Biol., 19: 1861-1872. doi:10.1111/j.1420-9101.2006.01171.x PMid:17040383

Koehn, R.K., R.I.E. Newell and F. Immermann. – 1980. Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc. Natl. Acad. Sci., 77: 5385-5389. doi:10.1073/pnas.77.9.5385

Kordos, L.M. and R.S Burton. – 1993. Genetic differentiation of Texas Gulf Coast populations of the blue crab Callinectes sapidus. Mar. Biol., 117: 227-233. doi:10.1007/BF00345667

Mantel, N. – 1967. The detection of disease clustering and a generalized regression approach. Cancer Res., 27: 209-220. PMid:6018555

Mariani, S., W. Hutchinson, E. Hatfield, D. Ruzzante, E. Simmonds, T. Dahlgren, C. Andre, J. Brigham, E. Torstensen and G. Carvalho.– 2005. North Sea herring population structure revealed by microsatellite analysis. Mar. Ecol. Prog. Ser., 303: 245-257. doi:10.3354/meps303245

Moksnes, P.-O., L. Pihl and J. van Montfrans. – 1998. Predation on postlarvae and juveniles of the shore crab Carcinus maenas: importance of shelter, size and cannibalism. Mar. Ecol. Prog. Ser., 166: 211-225. doi:10.3354/meps166211

Neal, K.J. and P.F. Pizzolla. – 2008. Carcinus maenas. Common shore crab. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. (http://www.marlin.ac.uk/species/Carcinusmaenas.htm).

Palumbi, S.R. – 2003. Population genetics, demographic connectivity, and the design of marine reserves. Ecol. Appl., 13(Suppl. 1): S146-S158. doi:10.1890/1051-0761(2003)013[0146:PGDCAT]2.0.CO;2

Pascoal, S., S. Creer, M.I. Taylor, H. Queiroga, G. Carvalho and S. Mendo. – 2009. Development and application of microsatellites in Carcinus maenas: genetic differentiation between northern and central Portuguese populations. PLoS ONE, 4(9): e7268. doi:10.1371/journal.pone.0007268 PMid:19789651    PMCid:2748716

Patarnello, T., F.A.M.J. Volckaert and R. Castilho. – 2007. Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol. Ecol., 16: 4426-4444. doi:10.1111/j.1365-294X.2007.03477.x PMid:17908222

Paula, J., I.C. Silva, S.M. Francisco and A.A.V. Flores. – 2006. The use of artificial benthic collectors for assessment of spatial patterns of settlement of megalopae of Carcinus maenas (L.) (Brachyura: Portunidae) in the lower Mira Estuary, Portugal. Hydrobiologia, 557: 69-77. doi:10.1007/s10750-005-1309-8

Peliz, A., P. Marchesiello, J. Dubert, M. Marta-Almeida, C. Roy and H. Queiroga. – 2007. A study of crab larvae dispersal on the Western Iberian Shelf: Physical processes. J. Mar. Syst., 68(1-2): 215-236. doi:10.1016/j.jmarsys.2006.11.007

Queiroga, H. – 1996. Distribution and drift of the crab Carcinus maenas (L.) (Decapoda, Portunidae) larvae over the continental shelf off northern Portugal in April 1991. J. Plankton Res., 18(11): 1981-2000. doi:10.1093/plankt/18.11.1981

Raymond, M. and F. Rousset. – 1995. genepop (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered., 86: 239.

Reuschel, S. and C.D. Schubart. – 2006. Phylogeny and geographic differentiation of Atlanto-Mediterranean species of the genus Xantho (Crustacea: Brachyura: Xanthidae) based on genetic and morphometric analyses. Mar. Biol., 148: 853-866. doi:10.1007/s00227-005-0095-1

Rohlf, F.J. and D.E. Slice. – 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool., 39: 40-59. doi:10.2307/2992207

Rohlf, F.J. – 2006. TpsDig, version 2.10. Stony Brook, NY: Department of Ecology and Evolution, State University of New York at Stony Brook.

Rohlf, F.J. – 2007a. TpsRelw, version 1.45. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.

Rohlf, F.J. – 2007b. TpsRegr, version 1.34. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.

Roman, J. and S.R. Palumbi. – 2004. A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol. Ecol., 13: 2891-2998. doi:10.1111/j.1365-294X.2004.02255.x PMid:15367106

Rousset, F. – 2001. Genetic approaches to the estimation of dispersal rates. In: J. Clobert, E. Danchin, A.A. Dhondt and J.D. Nichols (eds.), Dispersal, Oxford University Press, Oxford.

Rufino, M.M., P. Abelló and A.B. Yule. – 2004. Male and female carapace shape differences in Liocarcinus depurator (Decapoda, Brachyura): na application of geometric morphometric analysis to crustaceans. Italian J. Zool., 71: 79-83. doi:10.1080/11250000409356554

Schlichting, C.D. and M. Pigliucci. – 1998. Phenotypic Evolution: A reaction Norm Perspective, Sinauer Associates, Sunderland (MA).

Silva, I.C. and J. Paula. – 2008. Is there a better chela to use for geometric morphometric differentiation in brachyuran crabs? A case study using Pachygrapsus marmoratus and Carcinus maenas. J. Mar. Biol. Ass. UK, 88: 941-953. doi:10.1017/S0025315408001483

Silva, I.C., N. Mesquita, C.D. Schubart, M.J. Alves and J. Paula. – 2009. Genetic patchiness of the shore crab Pachygrapsus marmoratus along the Portuguese coast. J. Exp. Mar. Ecol. Biol., 378(1-2): 50-57. doi:10.1016/j.jembe.2009.07.032

Smith, L.D. – 2004. Biogeographic differences in claw size and performance in an introduced crab predator Carcinus maenas. Mar. Ecol. Prog. Ser., 276: 209-222. doi:10.3354/meps276209

Smith, L.D. and A. Palmer. – 1994. Effects of manipulated diet on size and performance of brachyuran crab claws. Science, 254: 710-712. doi:10.1126/science.264.5159.710 PMid:17737956

Tepolt, C.K., M.J. Bagley, J.B. Geller and M.J. Blum. – 2006. Characterization of microsatellite loci in the European green crab (Carcinus maenas). Mol. Ecol. Notes, 6: 343-345. doi:10.1111/j.1471-8286.2006.01226.x

Todd, P.A., R.A. Briers, R.J. Ladle and F. Middleton. – 2006. Phenotype-environment matching in the shore crab (Carcinus maenas). Mar. Biol., 148: 1357-1367. doi:10.1007/s00227-005-0159-2

Tresher, R., C. Proctor, G. Ruiz, R. Gurney, C. MacKinnon, W. Walton, L. Rodriguez and N. Bax. – 2003. Invasion dynamics of the European shore crab, Carcinus maenas, in Australia. Mar. Biol., 142: 867-876.

Trussell, G.C. – 1996. Phenotypic plasticity in an intertidal snail: The role of a common crab predator. Evolution, 50: 448-454. doi:10.2307/2410815

Trussell, G.C. and L.D. Smith. – 2000. Induced defenses in response to an invading crab predator: An explanation of historical and geographic phenotypic change. Proc. Natl. Acad. Sci., 97(5): 2123-2127. doi:10.1073/pnas.040423397 PMid:10681425

van Oosterhout, C., W.F. Hutchinson, D.P.M. Wills and P. Shipley. – 2004. micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes, 4: 535-538. doi:10.1111/j.1471-8286.2004.00684.x

Weir, B.S. and C.C. Cockerham. – 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. doi:10.2307/2408641

Yamada, S.B. – 2001. Global Invader: the European Green Crab. Oregon Sea Grant, Corvallis.

Zeng, C. and E. Naylor. – 1996. Endogenous tidal rhythms of vertical migration in field collected zoeal larvae of the shore crab Carcinus maenas: implications for ebb tide offshore dispersal. Mar. Ecol. Prog. Ser., 132: 71-82. doi:10.3354/meps132071




Copyright (c) 2010 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es