Abstract
The velvet swimming crab Necora puber is a common species along the European Atlantic coasts. Due to its increasing commercial importance, many studies have been carried out to characterize its growth and reproduction, but no genetic assessment has ever been attempted at the population level. Here, we describe the genetic diversity and population structure of N. puber in northwestern Spain (Galicia), including additional samples from France, Portugal, and southern Spain. To do so, we analysed two mitochondrial fragments of the COI and 16S genes in 217 individuals collected from ten localities. Our results unveil low-genetic diversity and weak population structure along the studied range. A range expansion after the last glacial maximum, followed by ongoing gene flow, seems to be the most likely explanation for the observed genetic pattern.
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References
Aboim MA, Menezes GM, Schlitt T, Rogers AD (2005) Genetic structure and history of populations of the deep-sea fish Helicolenus dactylopterus (Delaroche, 1809) inferred from mtDNA sequence analysis. Mol Ecol 14:1343–1354. doi:https://doi.org/10.1111/j.1365-294X.2005.02518.x
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. doi:https://doi.org/10.1109/TAC.1974.1100705
Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321. doi:https://doi.org/10.1016/S0169-5347(01)02151-6
Calderón I, Giribet G, Turon X (2008) Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Mar Biol (Berl) 154:137–151. doi:https://doi.org/10.1007/s00227-008-0908-0
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:https://doi.org/10.1046/j.1365-294x.2000.01020.x
Crease TJ (1999) The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:89–99. doi:https://doi.org/10.1016/S0378-1119(99)00151-1
Depraz A, Cordellier M, Hausser J, Pfenninger M (2008) Postglacial recolonization at a snail’s pace Trochulus villosus: confronting competing refugia hypotheses using model selection. Mol Ecol 17:2449–2462. doi:https://doi.org/10.1111/j.1365-294X.2008.03760.x
dos Santos A, Santos AMP, Conway DVP, Bartilotti C, Lourenço P, Queiroga H (2008) Diel vertical migration of decapod larvae in the Portuguese coastal upwelling ecosystem: implications for offshore transport. Mar Ecol Prog Ser 359:171–183. doi:https://doi.org/10.3354/meps07341
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. doi:https://doi.org/10.1046/j.1365-294X.2002.01650.x
Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864. doi:https://doi.org/10.1046/j.1365-294X.2003.02004.x
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
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 Biotechnol 3:294–299
Freire J, González-Gurriarán E (1995) Feeding ecology of the velvet swimming crab Necora puber in mussel raft areas of the Ría de Arousa (Galicia, NW Spain). Mar Ecol Prog Ser 119:139–154. doi:https://doi.org/10.3354/meps119139
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Garrick RC, Dyer RJ, Beheregaray LB, Sunnucks P (2008) Babies and bathwater: a comment on the premature obituary for nested clade phylogeographical analysis. Mol Ecol 17:1401–1403. doi:https://doi.org/10.1111/j.1365-294X.2008.03675.x
González-Gurriarán E (1985a) Crecimiento de la nécora Macropipus puber (L.) (Decapoda, Brachyura) en la Ría de Arousa (Galicia, NW España), y primeros datos sobre la dinámica de la población. Bol Inst Esp Oceanogr 2:33–51
González-Gurriarán E (1985b) Reproducción de la néocra Macropipus puber (L.) (Decapoda, Brachyura), y ciclo reproductivo en la Ría de Arousa (Galicia, NW España). Bol Inst Esp Oceanogr 2:10–32
Grant WAS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426. doi:https://doi.org/10.1093/jhered/89.5.415
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hasegawa M, Kishino H, Yano TA (1985) Dating of the human ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. doi:https://doi.org/10.1007/BF02101694
Hearn AR (2002) The transport chain of velvet crabs from Orkney, the Western Isles and Northumberland to Spain—a preliminary review. Seafish, pp 1–43
Hearn AR (2004) Reproductive biology of the velvet swimming crab, Necora puber (Brachyura, Portunidae), in the Orkney Islands, UK. Sarsia 89:318–325. doi:https://doi.org/10.1080/00364820410002578
Hickerson MJ, Cunningham CW (2000) Dramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Crustacea: Anomura). Mol Biol Evol 17:639–644
Ihssen PE, Booke HE, Casselman JM, McGlade JM, Payne NR, Utter FM (1981) Stock identification: materials and methods. Can J Fish Aquat Sci 38:1838–1855. doi:https://doi.org/10.1139/f81-230
Ketmaier V, Argano R, Caccone A (2003) Phylogeography and molecular rates of subterranean aquatic stenasellid isopods with a peri-Tyrrhenian distribution. Mol Ecol 12:547–555. doi:https://doi.org/10.1046/j.1365-294X.2003.01734.x
Knowles LL (2008) Why does a method that fails continue to be used? Evol Int J Org Evol 62:2713–2717. doi:https://doi.org/10.1111/j.1558-5646.2008.00481.x
Lee JT, Coleman RA, Jones MB (2005) Vertical migration during tidal transport of megalopae of Necora puber in coastal shallow waters during daytime. Estuar Coast Shelf Sci 65:396–404. doi:https://doi.org/10.1016/j.ecss.2005.05.022
Lee JT, Coleman RA, Jones MB (2006) Population dynamics and growth of juveniles of the velvet swimming crab Necora puber (Decapoda, Portunidae). Mar Biol (Berl) 148:609–619. doi:https://doi.org/10.1007/s00227-005-0107-1
Luttikhuizen PC, Campos J, Bleijswijk Jv, Peijnenburg KTCA, van der Veer HW (2008) Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range. Mol Phylogenet Evol 46:1015–1030. doi:https://doi.org/10.1016/j.ympev.2007.11.011
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Mantovani B, Scali V, Froglia C (1992) Allozymic characterization and phyletic relationships among four species of the genus Liocarcinus Stimpson, 1871 (Crustacea: Decapoda). Zool Anz 229:237–247
Miller AD, Murphy NP, Burridge CP, Austin CM (2005) Complete mitochondrial DNA sequences of the decapod crustaceans Pseudocarcinus gigas (Menippidae) and Macrobrachium rosenbergii (Palaemonidae). Mar Biotechnol 7:339–349. doi:https://doi.org/10.1007/s10126-004-4077-8
Narum S (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:https://doi.org/10.1007/s10592-005-9056-y
Neuenschwander S, Largiader CR, Ray N, Currat M, Vonlanthen P, Excoffier L (2008) Colonization history of the Swiss Rhine basin by the bullhead Cottus gobio: inference under a Bayesian spatially explicit framework. Mol Ecol 17:757–772
Palero F, Abelló P, Macpherson E, Gristina M, Pascual M (2008) Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Mol Phylogenet Evol 48:708–717. doi:https://doi.org/10.1016/j.ympev.2008.04.022
Passamonti M, Mantovani B, Scali V, Froglia C (1997) Genetic differentiation of European species of Liocarcinus (Crustacea: Portunidae): a gene–enzyme study. Zool Anz 235:157–247
Petit RJ (2008a) The coup de grâce for the nested clade phylogeographic analysis? Mol Ecol 17:516–518. doi:https://doi.org/10.1111/j.1365-294X.2008.03692.x
Petit RJ (2008b) On the falsifiability of the nested clade phylogeographic analysis method. Mol Ecol 17:1404. doi:https://doi.org/10.1111/j.1365-294X.2008.03692.x
Pfenninger M, Posada D (2002) Phylogeographic history of the land snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evol Int J Org Evol 56:1776–1788
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:https://doi.org/10.1093/bioinformatics/14.9.817
Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488. doi:https://doi.org/10.1046/j.1365-294x.2000.00887.x
Quinteiro J, Rodríguez-Castro J, Rey-Méndez M (2007) Population genetic structure of the stalked barnacle Pollicipes pollicipes (Gmelin, 1789) in the northeastern Atlantic: influence of coastal currents and mesoscale hydrographic structures. Mar Biol (Berl) 153:47–60. doi:https://doi.org/10.1007/s00227-007-0783-0
Ramírez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179:555–567. doi:https://doi.org/10.1534/genetics.107.083006
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898. doi:https://doi.org/10.1111/j.1365-294X.2004.02255.x
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:https://doi.org/10.1093/bioinformatics/btg359
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Schubart CD (2009) Mitochondrial DNA and decapod phylogenetics: the importance of pseudogenes and primer optimization. In: Martin JW, Crandall KA, Felder DL (eds) Crustacean issues 20. Decapod crustacean phylogenetics. Taylor & Francis/CRC Press, Boca Rato (in press)
Schubart CD, Neigel JE, Felder DL (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustac Issues 12:817–830
Segawa RD, Aotsuka T (2005) The mitochondrial genome of the Japanese freshwater crab, Geothelphusa dehaani (Crustacea: Brachyura): evidence for its evolution via gene duplication. Gene 355:28–39. doi:https://doi.org/10.1016/j.gene.2005.05.020
Sotelo G, Morán P, Fernández L, Posada D (2008) Genetic variation of the spiny spider crab Maja brachydactyla in the northeastern Atlantic. Mar Ecol Prog Ser 362:211–223. doi:https://doi.org/10.3354/meps07433
Strasser C, Barber P (2009) Limited genetic variation and structure in softshell clams (Mya arenaria) across their native and introduced range. Conserv Genet (in press)
Sun H, Zhou K, Song D (2005) Mitochondrial genome of the Chinese mitten crab Eriocheir japonica sinenesis (Brachyura: Thoracotremata: Grapsoidea) reveals a novel gene order and two target regions of gene rearrangements. Gene 349:207–217. doi:https://doi.org/10.1016/j.gene.2004.12.036
Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods). Version 4 beta 10. Sinauer Associates, Sunderland
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809. doi:https://doi.org/10.1046/j.1365-294X.2003.02041.x
Templeton AR (2008) Nested clade analysis: an extensively validated method for strong phylogeographic inference. Mol Ecol 17:1877–1880. doi:https://doi.org/10.1111/j.1365-294X.2008.03731.x
Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history—a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767–782
Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:https://doi.org/10.1093/nar/22.22.4673
Thorpe JP, Solé-Cava AM, Watts PC (2000) Exploited marine invertebrates: genetics and fisheries. Hydrobiologia 420:165–184. doi:https://doi.org/10.1023/A:1003987117508
Triant D, DeWoody J (2008) Molecular analyses of mitochondrial pseudogenes within the nuclear genome of arvicoline rodents. Genetica 132:21–33. doi:https://doi.org/10.1007/s10709-007-9145-6
Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420:191–201. doi:https://doi.org/10.1023/A:1003928327503
Watterson GA (1975) Number of segregating sites in genetic models without recombination. Theor Popul Biol 7:256–276. doi:https://doi.org/10.1016/0040-5809(75)90020-9
Williams ST, Knowlton N (2001) Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Mol Biol Evol 18:1484–1493
Williams ST, Jara J, Gomez E, Knowlton N (2002) The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr Comp Biol 42:941–952. doi:https://doi.org/10.1093/icb/42.5.941
Yamauchi MM, Miya MU, Nishida M (2003) Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura). Gene 311:129–135. doi:https://doi.org/10.1016/S0378-1119(03)00582-1
Acknowledgments
We are grateful to Jose Cuesta, Aitor Freire, Xurxo Gago, Daniel Latrouite and Antonina Santos for their help in obtaining samples, and to the Galician fishermen’s associations which kindly collected velvet crabs. We also thank Aida Ovejero for providing coastline distances, and Pilar Alvariño and Nieves Santamaría for lab assistance. Special thanks go to Rui Faria for helpful comments on an earlier version of this manuscript. This work was funded by a grant from the Xunta de Galicia (PGIDIT05RMA31001PR). Graciela Sotelo was supported by a pre-doctoral fellowship from the Xunta de Galicia. The experiments performed comply with the current laws.
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Sotelo, G., Posada, D. & Morán, P. Low-mitochondrial diversity and lack of structure in the velvet swimming crab Necora puber along the Galician coast. Mar Biol 156, 1039–1048 (2009). https://doi.org/10.1007/s00227-009-1148-7
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DOI: https://doi.org/10.1007/s00227-009-1148-7