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Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores

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Abstract

Variations in the relative contributions of gene flow and spatial and temporal variation in recruitment are considered the major determinants of population genetic structure in marine organisms. Such variation can be assessed through repeated measures of the genetic structure of a species over time. To test the relative importance of these two phenomena, temporal variation in genetic composition was measured in the limpet Cellana grata, among four annual cohorts over 10 years at four rocky shores in Hong Kong. A total of 408 limpets, comprising individuals from 1998, 1999, 2006 and 2007 cohorts were screened for genetic variation using five microsatellite loci. Minor but significant genetic differentiation was detected among samples from the 1998/1999 collection (F ST = 0.0023), but there was no significant differentiation among the 2006/2007 collection (F ST = 0.0008). Partitioning of genetic variation among shores was also significant in 1998/1999 but not in the 2006/2007 collection, although there was no correlation between genetic and geographic distances. There was no significant difference between collections made in 1998/1999 and 2006/2007. This lack of clear structure implies a high level of gene flow, but differentiation with time may be the result of stochastic recruitment variation among shores. Estimates of effective population size were not high (599, 95% C.L. 352–11397), suggesting the potential susceptibility of the populations to genetic drift, although a significant bottleneck effect was not detected. These findings indicate that genetic structuring between populations of C. grata in space and time may result from spatio-temporal variation in recruitment, but the potential development of biologically significant differentiation is suppressed by a lack of consistency in recruitment variability and high connectivity among shores.

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References

  • Ayata SD, Ellien C, Dumas F, Dubois S, Thiebaut E (2009) Modelling larval dispersal and settlement of the reef-building polychaete Sabellaria alveolata: role of hydroclimatic processes on the sustainability of biogenic reefs. Cont Shelf Res 29:1605–1623

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Faufaste N, Bonhomme F (2005) GENETIX v 4.05, logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Populations. CNRS UPR 9060, Université Montpellier II

  • Ben-Shlomo R, Douek J, Rinkevish B (2001) Heterozygote deficiency and chimerism in remote populations of a colonial ascidian from New Zealand. Mar Ecol Prog Ser 209:109–117

    Article  Google Scholar 

  • Bernal-Ramírez JH, Adcock GJ, Hauser L, Carvalho GR, Smith PJ (2003) Temporal stability of genetic population structure in the New Zealand snapper, Pagrus auratus, and relationship to coastal currents. Mar Biol 142:567–574

    Google Scholar 

  • Bhattacharya CG (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23:115–135

    Article  CAS  PubMed  Google Scholar 

  • Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186

    Article  CAS  PubMed  Google Scholar 

  • Botsford LW, Moloney CL, Hastings A, Largier JL, Powell TM, Higgins K, Quinn JF (1994) The influence of spatially and temporally varying oceanographic conditions on meroplanktonic metapopulations. Deep-sea Res Pt II 41:107–145

    Article  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    CAS  PubMed  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Article  Google Scholar 

  • Chan BKK, Williams GA (2004) Population dynamics of the acorn barnacles, Tetraclita squamosa and Tetraclita japonica (Cirripedia: Balanomorpha), in Hong Kong. Mar Biol 146:149–160

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  Google Scholar 

  • Corte-Real H, Hawkins S, Thorpe J (1996) Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries). Mar Biol 125:141–152

    Article  Google Scholar 

  • Costantini F, Fauvelot C, Abbiati M (2007) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser 340:109–119

    Article  CAS  Google Scholar 

  • David P, Perdieu MA, Pernot AF, Jarne P (1997) Fine-grained spatial and temporal population genetic structure in the marine bivalve Spisula ovalis. Evolution 51:1318–1322

    Article  Google Scholar 

  • De Aranzamendi MC, Sahade R, Tatian M, Chiappero MB (2008) Genetic differentiation between morphotypes in the Antarctic limpet Nacella concinna as revealed by inter-simple sequence repeat markers. Mar Biol 154:875–885

    Article  CAS  Google Scholar 

  • Di Rienzo A, Peterson AC, Garcza JC, Baldes AM, Slakin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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  PubMed  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Gaines SD, Bertness MD (1992) Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360:579–580

    Article  Google Scholar 

  • Gayanilo FCJ, Pauly D (1997) FAO/ICLARM stock assessment tools (FiSAT). Reference manual. FAO computer information series fisheries 8, 262 pp

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Gould AA (1859) Descriptions of shells collected by the North Pacific exploring expedition. Proc Boston Soc Nat Hist 7:40–166

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test for Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hawkins SJ, Hartnoll RG (1982) Settlement patterns of Semibalanus balanoides (L.) in the Isle of Man (1977–1981). J Exp Mar Biol Ecol 62:271–283

    Article  Google Scholar 

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

    Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hepburn RI, Sale PF, Dixon B, Heath DD (2009) Genetic structure of juvenile cohorts of bicolor damselfish (Stegastes partitus) along the Mesoamerican barrier reef: chaos through time. Coral Reefs 28:277–288

    Article  Google Scholar 

  • Hodgson AN, Le Quesne WJF, Hawkins SJ, Bishop JDD (2007) Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models. Mar Biol 150:415–426

    Article  Google Scholar 

  • Huang R (2001) Spatial variation in Cellana grata populations: the interplay of population dynamics and food availability. PhD thesis, The University of Hong Kong, Hong Kong

  • Jenkins GP, Black KP, Wheatley MJ, Hatton DN (1997) Temporal and spatial variability in recruitment of a temperate, seagrass-associated fish is largely determined by physical processes in the pre- and post-settlement phases. Mar Ecol Prog Ser 148:23–35

    Article  Google Scholar 

  • Johannesson K, Johannesson B, Lundgren U (1995) Strong natural selection causes microscale allozyme variation in a marine snail. Proc Natl Acad Sci USA 92:2602–2606

    Article  CAS  PubMed  Google Scholar 

  • Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164

    Article  Google Scholar 

  • Johnson MS, Black R (1984a) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38:1371–1383

    Article  Google Scholar 

  • Johnson MS, Black R (1984b) The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp. Mar Biol 79:295–302

    Article  Google Scholar 

  • Kordos LM, Burton RS (1993) Genetic differentiation of Texas Gulf Coast populations of the blue crab Callinectes sapidus. Mar Biol 117:227–233

    Article  Google Scholar 

  • Lambert WJ, Todd CD, Thorpe JP (2003) Genetic population structure of two intertidal nudibranch molluscs with contrasting larval types: temporal variation and transplant experiments. Mar Biol 142:461–471

    Google Scholar 

  • Lee HJ, Boulding EG (2007) Mitochondrial DNA variation in space and time in the northeastern Pacific gastropod, Littorina keenae. Mol Ecol 16:3084–3103

    Article  CAS  PubMed  Google Scholar 

  • Lenfant P, Planes S (2002) Temporal genetic changes between cohorts in a natural population of a marine fish, Diplodus sargus. Biol J Linn Soc 76:9–20

    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 

  • Liu JH (1994a) The ecology of the Hong Kong limpets Cellana grata (Gould, 1859) and Patelloida pygmaea (Dunker, 1860): reproductive biology. J Moll Stud 60:97–111

    Article  Google Scholar 

  • Liu JH (1994b) The ecology of the Hong Kong limpets Cellana grata (Gould, 1859) and Patelloida pygmaea (Dunker, 1860): distribution and population dynamics. J Moll Stud 60:55–67

    Article  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Lundy CJ, Rico C, Hewitt GM (2000) Temporal and spatial genetic variation in spawning grounds of European hake (Merluccius merluccius) in the Bay of Biscay. Mol Ecol 9:2067–2079

    Article  CAS  PubMed  Google Scholar 

  • Maes GE, Pujolar JM, Hellemans B, Volckaert FAM (2006) Evidence for isolation by time in the European eel (Anguilla anguilla L.). Mol Ecol 15:2095–2107

    Article  CAS  PubMed  Google Scholar 

  • Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868

    Article  CAS  PubMed  Google Scholar 

  • McIlwain JL (2003) Fine-scale temporal and spatial patterns of larval supply to a fringing reef in Western Australia. Mar Ecol Prog Ser 252:207–222

    Article  Google Scholar 

  • Morgan SG (2001) The larval ecology of marine communities. In: Bertness MD, Baines SD, Hay ME (eds) Marine community ecology. Sinauer Associates Inc., Sunderland, pp 159–181

    Google Scholar 

  • Ng WC, Chan MN, Slingsby G, Williams GA, Leung FCC (2009) Isolation and characterization of microsatellite markers from the limpet Cellana grata. Mol Ecol Resour 9:902–904

    Article  CAS  Google Scholar 

  • Ngan A (2006) Environmental stress and its implications for behavioural plasticity in foraging in Cellana grata. Unpublished PhD thesis, The University of Hong Kong, Hong Kong

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Pedersen EM, Hunt HL, Scheibling RE (2000) Temporal genetic heterogeneity within a developing mussel (Mytilus trossulus and M. edulis) assemblage. J Mar Biol Assoc UK 80:843–854

    Article  CAS  Google Scholar 

  • Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size, Version 1.3. Queensland Government, Department of Primary Industries and Fisheries

    Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: A software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pujolar JM, Maes GE, Volckaert FAM (2006) Genetic patchiness among recruits in the European eel Anguilla anguilla. Mar Ecol Prog Ser 307:209–217

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Raymond M, Vääntö RL, Thomas F, Rousset F, De Meeüs T, Renaud F (1997) Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Mar Ecol Prog Ser 156:225–237

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rose CG, Paynter KT, Hare MP (2006) Isolation by distance in the eastern oyster, Crassostrea virginica, in Chesapeake Bay. J Hered 97:158–170

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Svensson CJ, Jenkins SR, Hawkins SJ, Myers AA, Range P, Paula J, O’Riordan RM, Aberg P (2004) Models of open populations with space-limited recruitment in stochastic environments: relative importance of recruitment and survival in populations of Semibalanus balanoides. Mar Ecol Prog Ser 275:185–197

    Article  Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399

    CAS  PubMed  Google Scholar 

  • Turner TF, Wares JP, Gold JR (2002) Genetic effective size in three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 162:1329–1339

    PubMed  Google Scholar 

  • Underwood AJ, Fairweather PG (1989) Supply-side ecology and benthic marine assemblages. Trends Ecol Evol 4:16–20

    Article  Google Scholar 

  • van Oosterhaut C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Virgilio M, Abbiati M (2006) Temporal changes in the genetic structure of intertidal population of Hediste diversicolor (Polychaeta: Nereididae). J Sea Res 56:53–58

    Article  CAS  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    CAS  PubMed  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Weber LI, Hawkins LI (2006) Allozymic differentiation among geographically distant populations of Patella vulgata (Mollusca, Patellogastropoda). Hydrobiologia 553:267–275

    Article  CAS  Google Scholar 

  • Weetman D, Hauser L, Bayes MK, Ellis JR, Shaw PW (2006) Genetic population structure across a range of geographic scales in the commercially exploited marine gastropod Buccinum undatum. Mar Ecol Prog Ser 317:157–169

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103

    Article  Google Scholar 

  • Yan Y, Chan BKK, Williams WA (2006) Reproductive development of the barnacle Chthamalus malayensis in Hong Kong: implications for the life-history patterns of barnacles on seasonal, tropical shores. Mar Biol 148:875–887

    Article  Google Scholar 

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Acknowledgments

We thank M. N. Chan for microsatellite characterization, R.I. Lewis for his input during the early parts of this study and Neil Hutchinson for analysis of population structure. We are especially grateful to Michael Hellberg for constructive, critical comment on the MS. This research was supported by the Research Grants Council, Hong Kong (Project no. HKU7238/97M).

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Authors and Affiliations

  1. The Swire Institute of Marine Science and Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Pokfulam, Hong Kong

    Wai-Chuen Ng, Solomon T. C. Chak, G. Slingsby & Gray A. Williams

  2. School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Pokfulam, Hong Kong

    F. C. C. Leung

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  1. Wai-Chuen Ng
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  2. F. C. C. Leung
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  3. Solomon T. C. Chak
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  4. G. Slingsby
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Correspondence to Wai-Chuen Ng.

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Communicated by M. I. Taylor.

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Ng, WC., Leung, F.C.C., Chak, S.T.C. et al. Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores. Mar Biol 157, 325–337 (2010). https://doi.org/10.1007/s00227-009-1320-0

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