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Wide-spread genetic variability and the paradox of effective population size in the gag, Mycteroperca microlepis, along the West Florida Shelf

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Abstract

Wide-ranging marine species are often described as having a low effective population size (N e) to census size (N) ratio. This genetic phenomenon is typically attributed to large variation among individuals in reproductive success because of the high mortality rates and unpredictable environments associated with larval dispersal. In this study, we examined patterns of genetic variation in gag (Mycteroperca microlepis) on the West Florida Shelf across year classes of post-settlement juveniles and spawning adults. With no significant genetic differentiation among year classes despite varying recruitment dynamics, little evidence for chaotic genetic patchiness, and no truncation of adult genetic diversity in subsequent juvenile cohorts, there was little support for large variation among individual in reproductive success contributing to a low N e/N ratio. In fact, the consistent lack of significant differences in annual recruitment classes indicated that reproductive success among individuals was resistant to skewing. Among the various evolutionary forces that may be affecting N e, changes to demography due to fishing pressure are posited as a likely mechanism affecting current levels of genetic variation.

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References

  • Alter SE, Rynes E, Palumbi SR (2007) DNA evidence for historic population size and past ecosystem impacts of gray whales. Proc Natl Acad Sci USA 104:15162–15167. doi:10.1073/pnas.0706056104

    Article  CAS  Google Scholar 

  • Bagley MJ, Lindquist DG, Geller JB (1999) Microsatellite variation, effective population size, and population genetic structure of vermilion snapper, Rhomboplites aurorubens, off the southeastern USA. Mar Biol 134:609–620

    Article  CAS  Google Scholar 

  • Balloux F (2001) EASYPOP (version 1.7): a computer program for population genetics simulations. J Hered 92:301–302. doi:10.1093/jhered/92.3.301

    Article  CAS  Google Scholar 

  • Botsford LW, Micheli F, Hastings A (2003) Principles for the design of marine reserves. Ecol Appl 13:S25–S31

    Article  Google Scholar 

  • Buonaccorsi VP, Starkey E, Graves JE (2001) Mitochondrial and nuclear DNA analysis of population subdivision among young-of-the-year Spanish mackerel (Scomberomorus maculatus) from the western Atlantic and Gulf of Mexico. Mar Biol 138:37–45

    Article  CAS  Google Scholar 

  • Chapman RW, Sedberry GR, Koenig CC, Eleby BM (1999) Stock identification of gag, Mycteroperca microlepis, along the southeast coast of the United States. Mar Biotechnol 1:137–146

    Article  CAS  Google Scholar 

  • Coleman FC, Koenig CC, Collins LA (1996) Reproductive styles of shallow-water groupers (Pisces: Serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations. Environ Biol Fishes 47:129–141

    Article  Google Scholar 

  • Coleman FC, Figueira WF, Ueland JS, Crowder LB (2004) The impact of United States recreational fisheries on marine fish populations. Science 305:1958–1960

    Article  CAS  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  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 

  • Cushman EL, Jue NK, Strand AE, Sotka EE (2009) Evaluating the demographic significance of genetic homogeneity using a coalescent-based simulation: a case study with gag (Mycteroperca microlepis). Can J Fish Aquat Sci 66:1821–1830. doi:10.1139/f09-140

    Article  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. doi:10.1111/1755-0998.12157

    Article  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  CAS  Google Scholar 

  • Fitzhugh GR, Koenig CC, Coleman FC, Grimes CB, Sturges W (2005) Spatial and temporal patterns in fertilization and settlement of young gag (Mycteroperca microlepis) along the west Florida shelf. Bull Mar Sci 77:377–396

    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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gilbert-Horvath EA, Larson RJ, Garza JC (2006) Temporal recruitment patterns and gene flow in kelp rockfish (Sebastes atrovirens). Mol Ecol 15:3801–3815. doi:10.1111/j.1365-294X.2006.03033.x

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)

  • Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449. doi:10.1111/j.1523-1739.2010.01637.x

    Article  Google Scholar 

  • Harwood J, Stokes K (2003) Coping with uncertainty in ecological advice: lessons from fisheries. Trends Ecol Evol 18:617–622

    Article  Google Scholar 

  • Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362. doi:10.1111/j.1467-2979.2008.00299.x

    Article  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Ramirez JHB, Carvalho GR (2002) 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  CAS  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms?. Chapman and Hall, London

    Google Scholar 

  • Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc B Biol Sci 272:497–503. doi:10.1098/rspb.2004.2963

    Article  Google Scholar 

  • Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935

    Article  Google Scholar 

  • Jue NK (2006) Exploring the structure of genetic variation and the influences of demography on effective population size in the gag grouper Myteroperca microlepi (Goode & Bean). J Fish Biol 69:217–224. doi:10.1111/j.1095-8649.2006.01273.x

    Article  Google Scholar 

  • Koenig CC, Coleman FC (1998) Absolute abundance and survival of juvenile gags in sea grass beds of the Northeastern Gulf of Mexico. Trans Am Fish Soc 127:44–55

    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 

  • Lindberg WJ, Frazer TK, Portier KM, Vose F, Loftin J, Murie DJ, Mason DM, Nagy B, Hart MK (2006) Density-dependent habitat selection and performance by a large mobile reef fish. Ecol Appl 16:731–746

    Article  Google Scholar 

  • Lombardi-Carlson L, Fitzhugh G, Palmer C, Gardner C, Farsky R, Ortiz M (2008) Regional size, age and growth differences of red grouper (Epinephelus morio) along the west coast of Florida. Fish Res 91:239–251. doi:10.1016/j.fishres.2007.12.001

    Article  Google Scholar 

  • Lorenzen K (1996) The relationship between body weight and natural mortality in juvenile and adult fish: a comparison of natural ecosystems and aquaculture. J Fish Biol 49:627–647

    Article  Google Scholar 

  • Lotterhos KE, Markel RW (2012) Oceanographic drivers of offspring abundance may increase or decrease reproductive variance in a temperate marine fish. Mol Ecol 21:5009–5026. doi:10.1111/j.1365-294X.2012.12002.x

    Article  Google Scholar 

  • Macbeth GM, Broderick D, Buckworth RC, Ovenden JR (2013) Linkage disequilibrium estimation of effective population size with immigrants from divergent populations: a case study on Spanish Mackerel (Scomberomorus commerson). G3: Genes. Genomes Genet 3:709–717. doi:10.1534/g3.112.005124

    Google Scholar 

  • McGovern JC, Wyanski DM, Pashuk O, Manooch CS, Sedberry GR (1998) Changes in the sex ratio and size at maturity of gag, Mycteroperca microlepis, from the Atlantic coast of the southeastern United States during 1976–1995. Fish Bull 96:797–807

    Google Scholar 

  • McGovern JC, Sedberry GR, Meister HS, Westendorff TM, Wyanski DM, Harris PJ (2005) A tag and recapture study of gag, Mycteroperca microlepis, off the southeastern US. Bull Mar Sci 76:47–59

    Google Scholar 

  • Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402

    Article  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Mertz G, Myers RA (1996) Influence of fecundity on recruitment variability of marine fish. Can J Fish Aquat Sci 53:1618–1625

    Article  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    CAS  Google Scholar 

  • Mobley KB, Small CM, Jue NK, Jones AG (2010) Population structure of the dusky pipefish (Syngnathus floridae) from the Atlantic and Gulf of Mexico, as revealed by mitochondrial DNA and microsatellite analyses. J Biogeogr 37:1363–1377. doi:10.1111/j.1365-2699.2010.02288.x

    Article  Google Scholar 

  • Nunney L (1991) The influence of age structure and fecundity on effective population size. Pro R Soc Lond Ser B Biol Sci 246:71–76

    Article  CAS  Google Scholar 

  • Nunney L (1999) The effective size of a hierarchically structured population. Evolution 53:1–10

    Article  Google Scholar 

  • Palstra FP, Fraser DJ (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2:2357–2365. doi:10.1002/ece3.329

    Article  Google Scholar 

  • Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447. doi:10.1111/j.1365-294X.2008.03842.x

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158

    Article  Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

    Article  Google Scholar 

  • Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39. doi:10.1111/mec.12509

  • Pruett C, Saillant E, Gold J (2005) Historical population demography of red snapper (Lutjanus campechanus) from the northern Gulf of Mexico based on analysis of sequences of mitochondrial DNA. Mar Biol 147:593–602. doi:10.1007/s00227-005-1615-8

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Richardson LR, Gold JR (1997) Mitochondrial DNA diversity in and population structure of red grouper, Epinephelus morio, from the Gulf of Mexico. Fish Bull 95:174–179

    Google Scholar 

  • Rivera MAJ, Graham GC, Roderick GK (2003) Isolation and characterization of nine microsatellite loci from the Hawaiian grouper Epinephelus quernus (Serranidae) for population genetic analyses. Mar Biotechnol 5:126–129

    Article  CAS  Google Scholar 

  • Robinson JD, Moyer GR (2013) Linkage disequilibrium and effective population size when generations overlap. Evol Appl 6:290–302. doi:10.1111/j.1752-4571.2012.00289.x

    Article  Google Scholar 

  • Ruegg KC, Anderson EC, Baker CS, Vant M, Jackson JA, Palumbi SR (2010) Are Antarctic minke whales unusually abundant because of 20th century whaling? Mol Ecol 19:281–291. doi:10.1111/j.1365-294X.2009.04447.x

    Article  Google Scholar 

  • Ryman N (2006) CHIFISH: a computer program testing for genetic heterogeneity at multiple loci using Chi square and Fisher’s exact test. Mol Ecol Notes 6:285–287. doi:10.1111/j.1471-8286.2005.01146.x

    Article  Google Scholar 

  • Ryman N, Jorde PE (2001) Statistical power when testing for genetic differentiation. Mol Ecol 10:2361–2373

    Article  CAS  Google Scholar 

  • Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602

    Article  Google Scholar 

  • Saillant E, Gold JR (2006) Population structure and variance effective size of red snapper (Lutjanus campechanus) in the northern Gulf of Mexico. Fish Bull 104:136–148

    Google Scholar 

  • SEDAR (2006) SEDAR (southeast data assessment and review) 10: South Atlantic Gag Grouper. NOAA

  • SEDAR (2009) SEDAR (Southeast Data Assessment and Review) 10: Stock Assessment of Gag in the Gulf of Mexico: SEDAR Update Assessment NOAA

  • Switzer TS, MacDonald TC, McMichael RH Jr, Keenan SF (2012) Recruitment of juvenile gags in the eastern Gulf of Mexico and factor contributing to the observed spatial and temporal patterns of estuarine occupancy. Trans Am Fish Soc 141:707–719

    Article  Google Scholar 

  • Trexler JC, Travis J (2000) Can marine protected areas restore and conserve stock attributes of reef fishes? Bull Mar Sci 66:853–873

    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

    Google Scholar 

  • United States. National Marine Fisheries Service. Ecosystem Principles Advisory Panel (1998) Ecosystem-based fishery management: a report to Congress. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service

  • van OosterHout C, Hutchinson WF, Wills DPM, Shipley PF (2003) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352

    Article  CAS  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 (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 10:785–796. doi:10.1111/j.1755-0998.2010.02876.x

    Article  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262. doi:10.1111/j.1752-4571.2009.00104.x

    Article  Google Scholar 

  • Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189:633–644. doi:10.1534/genetics.111.132233

    Article  Google Scholar 

  • Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175:219–233. doi:10.1534/genetics.106.065300

    Article  Google Scholar 

  • Waples RS, Do C, Chopelet J (2011) Calculating N-e and N-e/N in age-structured populations: a hybrid Felsenstein–Hill approach. Ecology 92:1513–1522

    Article  Google Scholar 

  • Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics 146:427–441

    CAS  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  Google Scholar 

  • Zatcoff MS, Ball AO, Chapman RW (2002) Characterization of polymorphic microsatellite loci from black grouper, Mycteroperca bonaci (Teleostei : Serranidae). Mol Ecol Notes 2:217–219

    CAS  Google Scholar 

  • Zatcoff MS, Ball AO, Sedberry GR (2004) Population genetic analysis of red grouper, Epinephelus morio, and scamp, Mycteroperca phenax, from the southeastern US Atlantic and Gulf of Mexico. Mar Biol 144:769–777

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Joe Travis, Don Levitan, Peter Beerli, and Bill Landing for helpful comments on this manuscript and Robert Chapman and Amy Ball for all their help with the molecular methods. We would also like to thank the numerous people who volunteered their time, effort, and assistance in collecting samples: Jeff Taylor, Terry Doyle, DJ White, Ralph Woodring, Eric Milbrandt, Kendra Willet, Joe Pfaller, Richie Kuhar, Denise Akob, Chris Smith, Ashley Carter, Amy Grosgebauer, Holly Downing, Todd Bevis, Mia Adreani, Ben Ehrman, Heather Gamper, Mark Endries, Amanda Buchanan, Libby Carnahan, and Meaghan Darcy. Mr. Ed Ellison, Dr. Aaron Adams, Pat O’Donnell, and Dr. Bill Herrnkind must also be acknowledged for their particular contributions to the project. Overall, without the assistance of all these people, this work would never have been accomplished. We would like to acknowledge the Florida State University shared High-Performance Computing facility and staff for contributions to results presented in this paper. This research has been supported by grants from the National Marine Fisheries Service (NA04NMF4540213, NA07NMF4330120, NA17FF2876), the US Environmental Protection Agency’s Science to Achieve Results (STAR) program, the Disney National Wildlife Refuge Centennial Scholar program, and the Department of Biological Science at Florida State University and by the Florida State University Coastal and Marine Laboratory (FSUCML), the FSUCML Academic Diving Program, the NOAA-NMFS laboratory in Panama City, Mote Marine Laboratory, and the Rookery Bay National Estuarine Research Reserve.

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  1. Department of Biological Science, Florida State University, Tallahassee, FL, 32303, USA

    Nathaniel K. Jue, Felicia C. Coleman & Christopher C. Koenig

  2. Department of Molecular and Cell Biology, University of Connecticut, 354 Mansfield Rd., Storrs, CT, 06269, USA

    Nathaniel K. Jue

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  1. Nathaniel K. Jue
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  2. Felicia C. Coleman
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Correspondence to Nathaniel K. Jue.

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Jue, N.K., Coleman, F.C. & Koenig, C.C. Wide-spread genetic variability and the paradox of effective population size in the gag, Mycteroperca microlepis, along the West Florida Shelf. Mar Biol 161, 1905–1918 (2014). https://doi.org/10.1007/s00227-014-2473-z

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