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Maintenance of genetic variation and panmixia in the commercially exploited western rock lobster (Panulirus cygnus)

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Abstract

Marine species with high fecundities and mortalities in the early life stages can have low effective population sizes, making them vulnerable to declines in genetic diversity when they are commercially harvested. Here, we compare levels of microsatellite and mitochondrial sequence variation in the western rock lobster (Panulirus cygnus) over a 14-year period to test whether genetic variation is being maintained. Panulirus cygnus is a strong candidate for loss of genetic variation because it is a highly fecund species that is likely to experience high variance in reproductive success due to an extended larval planktonic stage. It also supports one of the largest and most economically important fisheries in Australia, with landings of between 8,000 and 14,500 tons (~70 % of the total legal-sized biomass) being harvested in some years. We found remarkably high levels of genetic variation in all samples and no evidence of a decline in genetic diversity over the time interval we studied. Furthermore, there was no evidence of a recent genetic bottleneck, and effective population size estimates based on single sample and temporal methods were infinitely large. Analysis of molecular variance indicated no significant population structure along 960 km of coastline or genetic differentiation among temporal samples. Our results support the view that P. cygnus is a single, panmictic population, and suggest genetic drift is not strong enough to reduce neutral genetic diversity in this species if current management practices and breeding stock sizes are maintained.

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References

  • Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23(6):327–337

    Article  PubMed  Google Scholar 

  • Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495

    Article  PubMed  CAS  Google Scholar 

  • Brown R (2009) Western rock lobster low puerulus settlement risk assessment workshop. Western Australian Department of Fisheries, Perth, Western Australia. URL: http://www.fish.wa.gov.au/docs/op/op071/fop71.pdf

  • Caputi N, Chubb C, Melville-Smith R, Pearce A, Griffin D (2003) Review of relationships between life history stages of the western rock lobster, Panularis cygnus, in Western Australia. Fish Res 65:47–61

    Article  Google Scholar 

  • Chittleborough RG (1974) Western rock lobster reared to maturity. Aust J Mar Fresh Res 25:221–225

    Article  Google Scholar 

  • Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297:94–96

    Article  PubMed  CAS  Google Scholar 

  • Consuegra S, Verspoor E, Knox D (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842

    Article  CAS  Google Scholar 

  • Cunningham CW, Blackstone NW, Buss LW (1992) Evolution of king crabs from hermit crab ancestors. Nature 355:539–542

    Article  PubMed  CAS  Google Scholar 

  • Cuveliers EL, Volckaert FAM, Rijnsdorp AD, Larmuseau MHD, Maes GE (2011) Temporal genetic stability and high effective population size despite fisheries-induced life-history trait evolution in the North Sea sole. Mol Ecol 20:3555–3568

    PubMed  CAS  Google Scholar 

  • Emerson BC (2007) Alarm bells for the molecular clock? No support for Ho et al.’s model of time-dependent molecular rate estimates. Syst Biol 56(2):337–345

    Article  PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Feng M, Slawinski D, Beckley LE, Keesing JK (2010) Retention and dispersal of shelf waters influenced by interactions of ocean boundary current and coastal geography. Mar Freshwater Res 61:1259–1267

    Article  CAS  Google Scholar 

  • Fletcher W, Chubb C, McCrea J, Caputi N, Webster F, Gould R, Bray T (2005) ESD Report Series No. 4—Western Rock Lobster Fishery. Perth, WA

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • García-Rodrguez FJ, Perez-Enriquez R (2008) Lack of genetic differentiation of blue spiny lobster Panulirus inflatus along the Pacific coast of Mexico inferred from mtDNA sequences. Mar Ecol Prog Ser 361:203–212

    Article  Google Scholar 

  • Gopal K, Tolley KA, Groeneveld JC, Matthee CA (2006) Mitochondrial DNA variation in spiny lobster Palinurus delagoae suggests genetically structured populations in the south-western Indian Ocean. Mar Ecol Prog Ser 319:191–198

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Accessed on 17 Nov 2009

  • Groth DM, Lim F, de Lestang SN, Beale N, Melville-Smith R (2009) Characterization of polymorphic microsatellite loci in the western rock lobster (Panulirus cygnus). Conserv Genet Resour 1:163–166

    Article  Google Scholar 

  • Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    PubMed  CAS  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Ramirez JHB, Carvalho GR (2003) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747

    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 and Hall, London, pp 122–134

    Google Scholar 

  • Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW et al (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc Lond 272:497–503

    Article  Google Scholar 

  • Hutchinson JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54:297–309

    Article  Google Scholar 

  • Hutchinson WF, van Oosterhout C, Rogers SI, Carvalho GR (2003) Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proc R Soc Lond 270:2125–2132

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Johnson MS, Wernham J (1999) Temporal variation of recruits as a basis of ephemeral genetic heterogeneity in the western rock lobster Panulirus cygnus. Mar Biol 135:133–139

    Article  Google Scholar 

  • Jørgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K et al (2007) Managing evolving fish stocks. Science 318:1247–1248

    Article  PubMed  Google Scholar 

  • Kambhampati S, Smith PT (1995) PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol Biol 4:233–236

    Article  PubMed  CAS  Google Scholar 

  • Kennington WJ, Levy E, Berry O, Groth DM, Waite AM, Johnson MS et al (2010) Characterization of 18 polymorphic microsatellite loci for the western rock lobster Panulirus cygnus. Conserv Genet Resour 2:389–391

    Article  Google Scholar 

  • Kuparinen A, Merilä J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659

    Article  PubMed  Google Scholar 

  • Luikart G, Allendorf FW, Sherwin B, Cornuet J-M (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 12:238–247

    Article  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and non-equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    PubMed  CAS  Google Scholar 

  • Melville-Smith R, de Lestang S (2006) Spatial and temporal variation in the size at maturity of the western rock lobster Panulirus cygnus George. Mar Biol 150:183–195

    Article  Google Scholar 

  • Miller LM, Kapuscinski AR (1997) Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 147:1249–1258

    PubMed  CAS  Google Scholar 

  • Morgan GR, Phillips B, Joll L (1982) Stock and recruitment relationships in Panulirus cygnus, the commercial rock (Spiny) lobster of Western Australia. Fish Bull 80:475–486

    Google Scholar 

  • Naro-Maciel E, Reid B, Holmes K, Brumbaugh D, Martin M, DeSalle R (2011) Mitochondrial DNA sequence variation in spiny lobsters: population expansion, panmixia, and divergence. Mar Biol 158(9):2027–2041

    Article  CAS  Google Scholar 

  • Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B et al (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935

    Article  PubMed  CAS  Google Scholar 

  • Ovenden JR, Brasher DJ, White RWG (1992) Mitochondrial DNA analyses of the red rock lobster Jasus edwardsii supports an apparent absence of population subdivision throughout Australasia. Mar Biol 112(2):319–326

    Article  CAS  Google Scholar 

  • Palero F, Abelló P, Macpherson E, Gristinad M, Pascual M (2008) Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Mol Phylo Evol 48: 708–717

    Google Scholar 

  • Palero F, Abelló P, Macpherson E, Beaumont M, Pascual M (2011) Effect of oceanographic barriers and overfishing on the population genetic structure of the European spiny lobster (Palinurus elephas). Biol J Linn Soc 104:407–418

    Article  Google Scholar 

  • Perez-Enriquez R, Vega A, Avila S, Sandoval JL (2001) Population genetics of red spiny lobster (Panulirus interruptus) along the Baja California Peninsula, Mexico. Mar Freshwater Res 52:1541–1549

    Article  Google Scholar 

  • Phillips BF (1986) Prediction of commercial catches of the western rock lobster Panulirus cygnus George. Can J Fish Aquat Sci 43:2126–2130

    Article  Google Scholar 

  • Phillips BF, Brown PA, Rimmev DW, Reid DD (1979) Distribution and dispersal of the phyllosoma larvae of the western rock lobster, Panulivus cygnus, in the south-eastern Indian Ocean. Aust J Mar Fresh Res 30:773–783

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2007). Documentation for STRUCTURE software: version 2.2. http://pritbsduchicagoedu/software/structure22/readmepdf

  • Riccioni G, Landi M, Ferrara G, Milano I, Cariani A, Zane L et al (2010) Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic Bluefin tuna of the Mediterranean Sea. Proc Natl Acad Sci USA 107(5):2102–2107

    Article  PubMed  CAS  Google Scholar 

  • Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446

    Article  Google Scholar 

  • Schubart CD, Diesel R, Hedges B (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365

    Article  CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Smith PJ, Francis RICC, McVeagh M (1991) Loss of genetic diversity due to fishing pressure. Fish Res 10:309–316

    Article  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson AP, Hanley JR, Johnson MS (1996) Genetic structure of the western rock lobster, Panulirus cygnus, with the benefit of hindsight. Mar Freshwater Res 47:889–896

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tolley KA, Groeneveld JC, Gopal K, Matthee CA (2005) Mitochondrial DNA panmixia in spiny lobster Palinurus gilchristi suggests a population expansion. Mar Ecol Prog Ser 297:225–231

    Article  CAS  Google Scholar 

  • Turner TF, Wares JP, Gold JR (2002) Genetic effective size is 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 

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

    Article  Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wright I, Caputi N, Penn J (2006) Depletion-based population estimates for western rock lobster (Panulirus cygnus) fishery in Western Australia. New Zeal J Mar Fresh 40:107–122

    Article  Google Scholar 

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Acknowledgments

We thank Amanda Worth and Sherralee Lukehurst for technical assistance, the Western Australian Department of Fisheries and the Department of Environment and Conservation for providing P. cygnus tissue samples and two anonymous reviewers for helpful comments on a previous version of this manuscript. This project was funded by the Fisheries Research and Development Corporation (project 2009/020).

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Authors and Affiliations

  1. School of Animal Biology, The University of Western Australia, Crawley, WA, 6009, Australia

    W. J. Kennington, S. A. Cadee, O. Berry & M. S. Johnson

  2. CSIRO Division of Marine and Atmospheric Research, Underwood Avenue, Floreat, WA, 6014, Australia

    O. Berry

  3. Curtin Health Innovation Research Institute, Biomedical Research Institute, Curtin University, GPO Box 1987, Perth, WA, 6845, Australia

    D. M. Groth

  4. Department of Environment and Agriculture, Curtin University, GPO Box 1987, Perth, WA, 6845, Australia

    R. Melville-Smith

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  1. W. J. Kennington
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  2. S. A. Cadee
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  3. O. Berry
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  4. D. M. Groth
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  5. M. S. Johnson
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  6. R. Melville-Smith
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Correspondence to W. J. Kennington.

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Kennington, W.J., Cadee, S.A., Berry, O. et al. Maintenance of genetic variation and panmixia in the commercially exploited western rock lobster (Panulirus cygnus). Conserv Genet 14, 115–124 (2013). https://doi.org/10.1007/s10592-012-0433-z

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