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Time and space: genetic structure of the cohorts of the common sea urchin Paracentrotus lividus in Western Mediterranean

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Abstract

Spatio-temporal variability in settlement and recruitment, high mortality during the first life-history stages, and selection may determine the genetic structure of cohorts of long-lived marine invertebrates at small scales. We conducted a spatial and temporal analysis of the common Mediterranean Sea urchin Paracentrotus lividus to determine the genetic structure of cohorts at different scales. In Tossa de Mar (NW Mediterranean), recruitment was followed over 5 consecutive springs (2006–2010). In spring 2008, recruits and two-year-old individuals were collected at 6 locations along East and South Iberian coasts separated from 200 to over 1,100 km. All cohorts presented a high genetic diversity based on a fragment of mtCOI. Our results showed a marked genetic homogeneity in the temporal monitoring and a low degree of spatial structure in 2006. In 2008, coupled with an abnormality in the usual circulation patterns in the area, the genetic structure of the southern populations studied changed markedly, with arrival of many private haplotypes. This fact highlights the importance of point events in renewing the genetic makeup of populations, which can only be detected through analysis of the cohort structure coupling temporal and spatial perspectives.

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References

  • Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Mol Phyl Evol 6:425–437

    Article  CAS  Google Scholar 

  • Banks SC, Piggot MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of false discovery rate under dependency. Ann Statist 29:1165–1188

    Article  Google Scholar 

  • Botsford LW, White JW, Coffroth MA, Paris CB, Planes S, Shearer TL, Thorrold SR, Jones GP (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical effort to predictive needs. Coral Reefs 28:327–337

    Article  Google Scholar 

  • Boudouresque CF, Verlaque M (2001) Ecology of Paracentrotus lividus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Tampa, FL, pp 177–215

    Chapter  Google Scholar 

  • Bouffard J, Pascual A, Ruiz S, Faugère Y, Tintoré J (2010) Coastal and mesoscale dynamics characterization using altimetry and gliders: a case study in the Balearic Sea. J Geophys Res 115:C10029. doi:10.1029/2009JC006087

    Article  Google Scholar 

  • Calderón I, Turon X (2010) Temporal genetic variability in the Mediterranean common sea urchin Paracentrotus lividus. Mar Ecol Prog Ser 408:149–159

    Article  Google Scholar 

  • Calderón I, Giribet G, Turon X (2008) Two markers and one history: phylogeography of the edible common sea urchin in the Lusitanian region. Mar Biol 154:137–151

    Article  Google Scholar 

  • Calderón I, Palacín C, Turon X (2009) Microsatellite markers fail to reveal genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in NW Mediterranean. Mol Ecol 18:3036–3049

    Article  Google Scholar 

  • Chao A, Shen TJ (2010) Program SPADE (Species Prediction And Diversity Estimation). Program and User’s Guide published at http://chao.stat.nthu.edu.tw

  • Chao A, Jost L, Chian SC, Jiang YH, Chazdon R (2008) A two-stage probabilistic approach to multiple-community similarity indices. Biometrics 64:1178–1186

    Article  Google Scholar 

  • Cowen RK, Lwiza KMM, Spongaule S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  Google Scholar 

  • Cushing DH (1990) Plankton production and year class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293

    Article  Google Scholar 

  • Duran S, Palacín C, Becerro MA, Turon X (2004) Genetic diversity and population structure of the commercially harvested sea urchin, Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328

    Article  CAS  Google Scholar 

  • Ebert TA (1983) Recruitment in echinoderms. Echinoderm Stud 1:169–203

    Google Scholar 

  • Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 126:443–450

    Article  CAS  Google Scholar 

  • Excoffier LG, Laval LG, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Flowers JM, Schroeter SC, Burton RS (2002) The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution 56:1445–1453

    CAS  Google Scholar 

  • Gosselin LA, Qian PY (1996) Early post-settlement mortality of an intertidal barnacle: a critical period for survival. Mar Ecol Prog Ser 135:69–75

    Article  Google Scholar 

  • Grosberg RK, Levitan DR (1992) For adults only? Supply-side and the life history of larval biology. Trends Ecol Evol 7:130–133

    Article  CAS  Google Scholar 

  • Guidetti P, Terlizzi A, Boero F (2004) Effects of the edible common sea urchin, Paracentrotus lividus, fishery along the Apulian rocky coast (SE Italy, Mediterranean Sea). Fish Res 66:287–297

    Article  Google Scholar 

  • Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment, editor and analysis program for windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrold C, Lisin S, Light KH, Tudor S (1991) Isolating settlement from recruitment of sea urchins. J Exp Mar Biol Ecol 147:1108–1116

    Article  Google Scholar 

  • Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull Mar Sci 39:550–564

    Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont A (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134

    Google Scholar 

  • Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79

    Article  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1683

    CAS  Google Scholar 

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Hereu B, Zabala M, Linares C, Sala E (2004) Temporal and spatial variability in settlement of the sea urchin Paracentrotus lividus in the NW Mediterranean. Mar Biol 144:1011–1018

    Article  Google Scholar 

  • Hogan JD, Thiessen RJ, Heath DD (2010) Variability in connectivity indicated by chaotic genetic patchiness within and among populations of a marine fish. Mar Ecol Prog Ser 417:263–275

    Article  Google Scholar 

  • Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301

    Article  Google Scholar 

  • Johnson MS, Holborn K, Black R (1993) Fine-scale patchiness and genetic heterogeneity of recruits of the corallivorous gastropod Drupella cornus. Mar Biol 117:91–96

    Article  Google Scholar 

  • Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  Google Scholar 

  • Jost L (2009) Gst versus D: reply to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

    Article  Google Scholar 

  • Levitan DR (2002) Density-dependent selection on gamete traits: are traits associated with fertilization related to sperm availability in three congeneric sea urchins? Ecology 83:464–479

    Article  Google Scholar 

  • Levitan DR (2004) Density-dependent sexual selection in external fertilizers: variances in male and female reproductive success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. Amer Natur 164:298–309

    Article  Google Scholar 

  • Levitan DR (2005) The distribution of male and female reproductive success in a broadcast spawning marine invertebrate. Integ Comp Biol 45:848–855

    Article  Google Scholar 

  • Li G, Hedgecock D (1998) Genetic heterogeneity, detected by PCR SSCP, among samples of larval Pacific oysters, (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Can J Fish Aquat Sci 55:1025–1033

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • López S, Turon X, Montero E, Palacín C, Duarte CM, Tarjuelo I (1998) Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea). Interannual variability and plankton-benthos coupling. Mar Ecol Prog Ser 172:239–251

    Article  Google Scholar 

  • López-Jurado JL, García Lafuente J, Pinot JM, Alvárez A (1996) Water exchanges in the Balearic channels. Bull Inst Océanogr Monaco 17. CIESM Sci Ser 2:41–63

    Google Scholar 

  • Lozano J, Galera J, López S, Turon X, Palacín C, Morera G (1995) Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:179–191

    Article  Google Scholar 

  • Maltagliati F, Di Giuseppe G, Barbieri M, Castelli A, Dini F (2010) Phygeography and genetic structure of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) inferred from the mitochondrial cytochrome b gene. Biol J Linn Soc 100:910–923

    Article  Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Ecol Resour 11:5–18

    Article  Google Scholar 

  • Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397–406

    CAS  Google Scholar 

  • Moberg PE, Burton RS (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 136:773–784

    Article  CAS  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Olivar P, Catalán IA, Emelianov M, Fernández de Puelles ML (2003) Early stages of Sardina pilchardus and environmental anomalies in the Northwestern Mediterranean. Estuar Coast Shelf Sci 56:609–619

    Article  Google Scholar 

  • Ourens R, Fernández L, Freire J (2011) Geographic, population, and seasonal patterns in the reproductive parameters of the sea urchin Paracentrotus lividus. Mar Biol 158:793–804

    Article  Google Scholar 

  • Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. PNAS USA 96:12632–12637

    Article  CAS  Google Scholar 

  • Palumbi SR, Wilson AC (1990) Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis. Evolution 44:403–415

    Article  Google Scholar 

  • Pascual A, Buongiorno Nardelli B, Larnicol G, Emelianov M, Gomis D (2002) A case of an intense anticyclonic eddy in the Balearic Sea (Western Mediterranean). J Geophys Res 107:3183–3196

    Article  Google Scholar 

  • Pedrotti ML (1993) Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. J Mar Biol Assoc UK 73:513–530

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pini J, Planes S, Rochel E, Lecchini D, Fauvelot C (2011) Genetic diversity loss associated to high mortality and environmental stress during the recruitment stage of a coral reef fish. Coral Reefs 30:1–6

    Article  Google Scholar 

  • Pinot JM, López-Jurado JL, Riera M, Jansà J, Font J, Tintoré J (1998) Time flow variability in the Balearic channels and its relevance to the western Mediterranean circulation. Rapp Comm Int Mer Médit 35:188–189

    Google Scholar 

  • Planes S, Lenfant P (2002) Temporal change in the genetic structure between and within cohorts of a marine fish, Diplodus sargus, induced by a large variance in individual reproductive success. Mol Ecol 11:1515–1524

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds). Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ, pp 365–386. Source code available at http://fokker.wi.mit.edu/primer3/

  • Ryman N, Leimar O (2009) G ST is still a useful measure of genetic differentiation—a comment on Jost’s D. Mol Ecol 18:2084–2087

    Article  Google Scholar 

  • Selkoe KA, Gaines SD, Caselle JE, Warner RR (2006) Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 87:3082–3094

    Article  Google Scholar 

  • Sponaugle S, Cowen EK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375

    Google Scholar 

  • Tomas F, Romero J, Turon X (2004) Settlement and recruitment of the sea urchin Paracentrotus lividus in two contrasting habitats in the Mediterranean. Mar Ecol Prog Ser 282:173–184

    Article  Google Scholar 

  • Turon X, Giribet G, López S, Palacín C (1995) Growth and population structure of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:193–204

    Article  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Amer Genet Assoc 89:438–450

    Google Scholar 

  • Watts RJ, Johnson MS, Black R (1990) Effects of recruitment on genetic patchiness in the sea urchin Echinometra mathaei in Western Australia. Mar Biol 105:145–151

    Article  Google Scholar 

  • Zigler KS, McCartney MA, Levitan DR, Lessios HA (2005) Sea urchin bindin divergence predicts gamete compatibility. Evolution 59:2399–2404

    Google Scholar 

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Acknowledgments

Special thanks to Gonzalo Giribet for his help during sampling. Thanks also to Owen Wangensteen, to Nuria Massana, and to Andrea Soriano for their help during separation of recruits. We are in debt to Joaquín Tintoré and Ananda Pascual for providing and discussing information upon currents and transport of particles. This research was funded by projects CTM2010-2218 of the Spanish Ministry of Science and Innovation and BIOCON08-187 of the Foundation of the BBVA banking institution.

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Communicated by T. Reusch.

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Calderón, I., Pita, L., Brusciotti, S. et al. Time and space: genetic structure of the cohorts of the common sea urchin Paracentrotus lividus in Western Mediterranean. Mar Biol 159, 187–197 (2012). https://doi.org/10.1007/s00227-011-1799-z

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