Conservation Genetics

, Volume 15, Issue 1, pp 109–121 | Cite as

Development and application of genomic tools to the restoration of green abalone in southern California

  • K. M. Gruenthal
  • D. A. Witting
  • T. Ford
  • M. J. Neuman
  • J. P. Williams
  • D. J. PondellaII
  • A. Bird
  • N. Caruso
  • J. R. Hyde
  • L. W. Seeb
  • W. A. Larson
Research Article
First Online:
Received:
Accepted:

Abstract

Due to severe declines in abundance throughout southern California, the green abalone (Haliotis fulgens Philippi 1845) became protected under a state-sponsored fishery moratorium in 1997 and was declared a NOAA NMFS Species of Concern in 2004. Recently, H. fulgens was chosen for possible stock restoration via translocation of wild adults to depleted habitat and supplementation through releasing cultured individuals. Before a management plan could be developed, however, an understanding of the species’ natural population genetic structure was needed. We used a genomic technique called restriction site associated DNA sequencing (RADSeq) to address the issue. RADSeq enabled discovery of 1,209 single nucleotide polymorphisms theoretically spread genome-wide in H. fulgens. Analyses suggested the species may be panmictic throughout our sampled range, with an effective population size (Ne) of 1,100–3,600. Hence, limitations to management, such as requiring local broodstock and restricting translocation potential, might be unnecessary. Sites with larger populations may be suitable sources for restoration of depleted sites (e.g. the Palos Verdes Peninsula), although the extent of local adaptation remains unknown. Despite this potential for restoration, results gathered on a sample of cultured H. fulgens illustrated how quickly genetic diversity can be lost through captive breeding. To help mitigate a drop in Ne due to hatchery supplementation, we recommend collection and replacement of ≥100 wild abalone per generation for broodstock and close management of the proportion of cultured individuals in the wild. Successful implementation will depend on operational capacity and the resilience of the source populations to broodstock collection.

Keywords

Abalone Genomics Population genetics Restriction site associated DNA sequencing Single nucleotide polymorphism Stock enhancement 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by the U.S. Department of Commerce’s National Oceanic and Atmospheric Administration (NOAA) under a Species of Concern Internal Grant awarded to Ford et al. and an Office of Aquaculture Research Tiger Team Internal Grant awarded to Dr. Hyde. Wesley Larson was supported by a National Science Foundation Graduate Research Fellowship Grant # DGE-0718124. The views expressed herein do not necessarily reflect the views of those organizations. Tissue from wild H. fulgens was collected by the authors, as well as Brian Meux, Ray Hiemstra, and several staff. The SEA Lab sample was provided by Brent Scheiwe. Dr. Jim Seeb at the University of Washington provided guidance and laboratory space. We would like to thank Seeb Lab members Carita Pascal for lab instruction and Ryan Waples for help initiating the Stacks pipeline. We would also like to thank Drs. Fred Utter, Brent Vadopalas, and Robin Waples and two anonymous reviewers for valuable commentary on this manuscript.

Supplementary material

10592_2013_524_MOESM1_ESM.xlsx (456 kb)
Supplementary material 1 (XLSX 455 kb)

References

  1. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190CrossRefGoogle Scholar
  2. Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 18:1507–1514CrossRefGoogle Scholar
  3. Allendorf FW, Ryman N (1987) Genetic management of hatchery stocks. In: Ryman N, Utter F (eds) Population genetics and fishery management. University of Washington Press, Seattle, pp 141–159Google Scholar
  4. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709PubMedCrossRefGoogle Scholar
  5. Araki H, Schmid C (2010) Is hatchery stocking a help or harm? Evidence, limitations and future direction in ecological and genetic surveys. Aquaculture 308:S2–S11CrossRefGoogle Scholar
  6. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376. doi: 10.1371/journal.pone.0003376 PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bray NA, Keyes A, Morawitz WML (1999) The California current system in the southern California Bight and the Santa Barbara Channel. J Geophys Res 104:7695–7714CrossRefGoogle Scholar
  8. Burton RS, Tegner MJ (2000) Enhancement of red abalone Haliotis rufescens stocks at San Miquel Island: reassessing a success story. Mar Ecol Prog Ser 202:303–308CrossRefGoogle Scholar
  9. California Department of Fish and Game (CDFG), Marine Region (2005) Abalone recovery and management plan, final. The Resources Agency, SacramentoGoogle Scholar
  10. Camara MD, Vadopalas B (2009) Genetic aspects of restoring Olympia oysters and other native bivalves: balancing good intentions, the need for action, and the risks of making things worse. J Shellfish Res 28:121–145CrossRefGoogle Scholar
  11. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. Genes Genomes Genet 1:171–182Google Scholar
  12. Catchen JM, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140PubMedCrossRefGoogle Scholar
  13. Chambers MD, VanBlaricon GR, Hauser L, Utter F, Friedman CS (2006) Genetic structure of black abalone (Haliotis cracherodii) populations in the California islands and central California coast: impacts of larval dispersal and decimation from withering syndrome. J Exp Mar Biol Ecol 331:173–185CrossRefGoogle Scholar
  14. Cross TF, King J (1983) Genetic-effects of hatchery rearing in Atlantic salmon. Aquaculture 33:33–40CrossRefGoogle Scholar
  15. Davey JW, Blaxter ML (2010) RADSeq: next-generation population genetics. Brief Funct Genomics 9:416–423Google Scholar
  16. De Wit P, Palumbi SR (2013) Transcriptome-wide polymorphisms of red abalone (Haliotis rufescens) reveal patterns of gene flow and local adaptation. Mol Ecol 22:2884–2897PubMedCrossRefGoogle Scholar
  17. Díaz-Viloria N, Cruz P, Guzmán-Del Próo SA, Perez-Enriquez R (2009) Genetic connectivity among pink abalone Haliotis corrugata populations. J Shellfish Res 28:599–608CrossRefGoogle Scholar
  18. Duchesne P, Bernatchez L (2002) An analytical investigation of the dynamics of inbreeding in multi-generation supportive breeding. Conserv Gen 3:47–60CrossRefGoogle Scholar
  19. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Gen Res 4:359–361CrossRefGoogle Scholar
  20. Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci 107:16196–16200PubMedCrossRefGoogle Scholar
  21. Etter PD, Preston JL, Bassham S, Cresko WA, Johnson EA (2011) Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE 6:e18561. doi: 10.1371/journal.pone.0018561 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  23. Evans B, Barlett J, Sweijd N, Cook P, Elliot NG (2004a) Loss of genetic variation at microsatellite loci in hatchery produced abalone in Australia (Haliotis rubra) and South Africa (Haliotis midae). Aquaculture 233:109–127CrossRefGoogle Scholar
  24. Evans BS, Sweijd NA, Bowie RCK, Cook PA, Elliot NG (2004b) Population genetic structure of the perlemoen Haliotis midae in South Africa: evidence of range expansion and founder events. Mar Ecol Prog Ser 270:163–172CrossRefGoogle Scholar
  25. Everett MV, Miller MR, Seeb JE (2012) Meiotic maps of sockeye salmon derived from massively parallel DNA sequencing. BMC Genomics 13:521PubMedCentralPubMedCrossRefGoogle Scholar
  26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  27. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCentralPubMedCrossRefGoogle Scholar
  28. Fisch KM, Ivy JA, Burton RS, May B (2013) Evaluating the performance of captive breeding techniques for conservation hatcheries: a case study of the Delta Smelt Captive Breeding Program. J Hered 104:92–104PubMedCrossRefGoogle Scholar
  29. Fischer MC, Foll M, Excoffier L, Heckel G (2011) Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Mol Ecol 20:1450–1462PubMedCrossRefGoogle Scholar
  30. Florida Fish and Wildlife Conservation Commission (FWC) (2007) Genetic policy for the release of finfishes in Florida. Publication Number IHR-2007-001. FWC FWRI, TallahasseeGoogle Scholar
  31. Foll M, Gaggiotti OE (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993PubMedCrossRefGoogle Scholar
  32. Foll M, Fischer MC, Heckel G, Excoffier L (2010) Estimating population structure from AFLP amplification intensity. Mol Ecol 19:4638–4647PubMedCrossRefGoogle Scholar
  33. Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, CambridgeGoogle Scholar
  34. Franklin IR (1980) Evolutionary change in small populations. In: Soulé M, Wilcox B (eds) Conservaiton biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 135–149Google Scholar
  35. Gagnaire P-A, Normandeau E, Pavey SA, Bernatchez L (2013) Mapping phenotypic, expression and transmission ratio distortion QTL using RAD markers in the Lake Whitefish (Coregonus clupeaformis). Mol Ecol 22:3036–3048PubMedCrossRefGoogle Scholar
  36. Gao X, Martin ER (2009) Using allele sharing distance for detecting human population stratification. Hum Hered 68:182–191PubMedCrossRefGoogle Scholar
  37. Gao X, Starmer J (2007) Human population structure analysis via multilocus genotype clustering. BMC Genet 8:34PubMedCentralPubMedCrossRefGoogle Scholar
  38. Gao X, Starmer J (2008) AWclust: point-and-click software for non-parametric population structure analysis. BMC Bioinform 9:77CrossRefGoogle Scholar
  39. Gaylord B, Reed DC, Washburn L, Raimondi PT (2004) Physical–biological coupling in spore dispersal of kelp forest macroalgae. J Mar Syst 49:19–39CrossRefGoogle Scholar
  40. Geiger DL (2000) Distribution and biogeography of the recent Haliotidae (Gastropoda: Vetigastropoda) worldwide. Boll Malacol 35:57–120Google Scholar
  41. Gruenthal KM (2007) Conservation genetics of California abalone species. Dissertation, University of California at San Diego, La JollaGoogle Scholar
  42. Gruenthal KM, Burton RS (2008) Genetic structure of natural populations of the California black abalone (Haliotis cracherodii Leach, 1814), a candidate for endangered species status. J Exp Mar Biol Ecol 355:47–58CrossRefGoogle Scholar
  43. Gruenthal KM, Acheson LK, Burton RS (2007) Genetic structure of natural populations of California red abalone (Haliotis rufescens) using multiple genetic markers. Mar Biol 152:1237–1248CrossRefGoogle Scholar
  44. Gutiérrez-Gonzalez JL, Perez-Enriquez R (2005) A genetic evaluation of stock enhancement of blue abalone Haliotis fulgens in Baja California, Mexico. Aquaculture 247:233–242CrossRefGoogle Scholar
  45. Gutiérrez-Gonzalez JL, Cruz P, del Rio-Portilla MA, Perez-Enriquez R (2007) Genetic structure of green abalone Haliotis fulgens population off Baja California, Mexico. J Shellfish Res 26:839–846CrossRefGoogle Scholar
  46. Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS ONE 7:e45170. doi: 10.1371/journal.pone.0045170 PubMedCentralPubMedCrossRefGoogle Scholar
  47. Hara M, Sekino M (2007) Genetic differences between hatchery stocks and natural populations in Pacific abalone (Haliotis discus) estimated using microsatellite DNA markers. Mar Biotechnol 9:74–81PubMedCrossRefGoogle Scholar
  48. Hemmer-Hansen J, Nielsen EE, Therkildsen NO, Taylor MI, Ogden R, Geffen AJ, Bekkevold D, Helyar S, Pampoulie C, Johansen T, FishPopTrace Consortium, Carvalho GR (2013) A genomic island linked to ecotype divergence in Atlantic cod. Mol Ecol 22:2653–2667PubMedCrossRefGoogle Scholar
  49. Hobday AJ, Tegner MJ, Haaker PL (2001) Over-exploitation of a broadcast spawning marine invertebrate: decline of the white abalone. Rev Fish Biol Fish 10:493–514CrossRefGoogle Scholar
  50. Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G (2011) Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Resour 11:117–122PubMedCrossRefGoogle Scholar
  51. Hohenlohe PA, Day MD, Amish SJ, Miller MR, Kamps-Hughes N, Boyer MC, Muhlfeld CC, Allendorf FW, Johnson EA, Luikart G (2013) Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Mol Ecol 22:3002–3013PubMedCrossRefGoogle Scholar
  52. Huang XQ, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877PubMedCrossRefGoogle Scholar
  53. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCentralPubMedCrossRefGoogle Scholar
  54. Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv Genet 7:991–995CrossRefGoogle Scholar
  55. Kincaid HL (1983) Inbreeding in fish populations used for aquaculture. Aquaculture 33:215–227CrossRefGoogle Scholar
  56. Lapota D, Rosen G, Chock J, Liu CH (2000) Red and green abalone seed grow out for reseeding activities off Point Loma, California. J Shellfish Res 19:431–438Google Scholar
  57. Leighton DL (2000) The biology and culture of the California abalones. Dorrance Publishing Co., Inc., PhiladelphiaGoogle Scholar
  58. Lemay MA, Boulding EG (2009) Microsatellite pedigree analysis reveals high variance in reproductive success and reduced genetic diversity in hatchery-spawned northern abalone. Aquaculture 295:22–29CrossRefGoogle Scholar
  59. Letcher BH, King TL (1999) Targeted stock identification using multilocus genotype ‘familyprinting’. Fish Res 43:99–111CrossRefGoogle Scholar
  60. LeVay L, Carvalho GR, Quinitio ET, Lebata JH, Ut VN, Fushimi J (2007) Quality of hatchery-reared juveniles for marine fisheries stock enhancement. Aquaculture 269:169–180CrossRefGoogle Scholar
  61. Li Q, Kijima A (2006) Genetic variation of Chinese and Japanese wild Pacific abalone (Haliotis discus hannai) measured by microsatellite DNA markers. Acta Oceanol Sin 25:146–155Google Scholar
  62. Miller LM, Kapuscinski AR (2003) Genetic guidelines for hatchery supplementation programs. In: Hallerman EM (ed) Population genetics: principles and practices for fisheries scientists. American Fisheries Society, Bethesda, pp 329–355Google Scholar
  63. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518CrossRefGoogle Scholar
  64. Miner CM, Alstatt JM, Raimondi PT, Minchinton TE (2007) Recruitment failure and shifts in community structure following mass mortality limit recovery prospects of black abalone. Mar Ecol Prog Ser 327:107–117CrossRefGoogle Scholar
  65. Moyle PB, Israel JA, Purdy SE (2008) Salmon, steelhead, and trout in California: status of an emblematic fauna. Center for Watershed Sciences, University of California at Davis, DavisGoogle Scholar
  66. Narum SR, Hess JE (2011) Comparison of FST outlier tests for SNP loci under selection. Mol Ecol Resour 11:184–194PubMedCrossRefGoogle Scholar
  67. National Marine Fisheries Service (NMFS) (2008) White abalone recovery plan (Haliotis sorenseni). National Oceanic and Atmospheric Administration (NOAA) NMFS Regional Office, Long BeachGoogle Scholar
  68. Neuman M, Tissot B, VanBlaricom G (2010) Overall status and threats assessment of black abalone (Haliotis cracherodii Leach, 1814) populations in California, USA. J Shellfish Res 29:577–586CrossRefGoogle Scholar
  69. Ovenden JR, Peel D, Street R, Courtney AJ, Hoyle SD, Peel SL, Podlich H (2007) The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol 16:127–138PubMedCrossRefGoogle Scholar
  70. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  71. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539PubMedCrossRefGoogle Scholar
  72. Peel D, Waples RS, Macbeth GM, Do C, Ovenden JR (2012) Accounting for missing data in the estimation of contemporary genetic effective population size (Ne). Mol Ecol Res 13:243–253CrossRefGoogle Scholar
  73. Pella JJ, Milner GB (1987) Use of genetic marks in stock composition analysis. In: Ryman N, Utter F (eds) Population genetic and fisheries management. University of Washington Press, Seattle, pp 247–276Google Scholar
  74. Prince JD, Sellers TL, Ford WB, Talbot SR (1987) Experimental evidence for limited dispersal of haliotid larvae (genus Haliotis; Mollusca: Gastropoda). J Exp Mar Biol Ecol 106:243–263CrossRefGoogle Scholar
  75. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  76. Reitzel AM, Herrera S, Layden MJ, Martindale MQ, Shank TM (2013) Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol Ecol. doi: 10.1111/mec.12228 PubMedGoogle Scholar
  77. Remshardt J, Turner T, Perez T, Ulibarri M, Hines P, Altenbach C, Keeler-Foster C, Osborne M, Caldwell C, Parody J (2009) Rio Grande silvery minnow genetic management and propagation plan. Middle Rio Grande Endangered Species Collaborative Program. http://middleriogrande.com/LinkClick.aspx?fileticket=nAj3x8zOMgA%3d&tabid=218&mid=1131. Accessed 21 Mar 2013
  78. Roesti M, Salzburger W, Berner D (2012) Uninformative polymorphisms bias genome scans for signatures of selection. BMC Evol Biol 12:94–100PubMedCentralPubMedCrossRefGoogle Scholar
  79. Rogers-Bennett L, Allen BL, Davis GE (2004) Measuring abalone (Haliotis spp.) recruitment in California to examine recruitment overfishing and recovery criteria. J Shellfish Res 23:1201–1207Google Scholar
  80. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefGoogle Scholar
  81. Rubin BER, Ree RH, Moreau CS (2012) Inferring phylogenies from RAD sequence data. PLoS ONE 7:e33394. doi: 10.1371/journal.pone.0033394 PubMedCentralPubMedCrossRefGoogle Scholar
  82. Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329CrossRefGoogle Scholar
  83. Ryman N, Jorde PE, Laikre L (1995) Supportive breeding and variance effective size. Conserv Biol 9:1619–1628CrossRefGoogle Scholar
  84. San Joaquin River Restoration Program (SJRRP) (2010) Hatchery and genetic management plan: San Joaquin River Salmon Conservation and Research FacilityGoogle Scholar
  85. Sekino M, Takahiro S, Fujita T, Kobayashi T, Takami H (2005) Microsatellite DNA markers of Ezo abalone (Haliotis discus hannai): a preliminary assessment of natural populations sampled from heavily stocked areas. Aquaculture 243:33–47CrossRefGoogle Scholar
  86. Slabbert R, Bester AE, D’Amato ME (2009) Analyses of genetic diversity and parentage within a South African hatchery of the abalone Haliotis midae Linnaeus using microsatellite markers. J Shellfish Res 28:369–375CrossRefGoogle Scholar
  87. Smith PJ, Conroy AM (1992) Loss of genetic variation in hatchery-produced abalone, Haliotis iris. N Z J Mar Fresh Res 26:81–85CrossRefGoogle Scholar
  88. Tang S, Popongviwat A, Klinbunga S, Tassanakajon A, Jarayabhand P, Menasveta P (2005) Genetic heterogeneity of the tropical abalone (Haliotis asinina) revealed by RAPD and microsatellite analysis. J Biochem Mol Biol 38:182–190PubMedCrossRefGoogle Scholar
  89. Taniguchi N (2003) Genetic factors in broodstock management for seed production. Rev Fish Biol Fish 13:177–185CrossRefGoogle Scholar
  90. Tegner MJ, Butler RA (1985) Drift-tube study of the dispersal potential of green abalone (Haliotis fulgens) larvae in the southern California Bight: implications for recovery of depleted populations. Mar Ecol Prog Ser 26:73–84CrossRefGoogle Scholar
  91. Temby N, Miller K, Mundy C (2007) Evidence of genetic subdivision among populations of blacklip abalone (Haliotis rubra Leach) in Tasmania. Mar Freshw Res 58:733–742CrossRefGoogle Scholar
  92. Travis J, Coleman FC, Grimes CB, Conover D, Bert TM, Tringali M (1998) Critically assessing stock enhancement: an introduction to the Mote Symposium. Bull Mar Sci 62:305–311Google Scholar
  93. Tringali MD (2006) A Bayesian approach for the genetic tracking of cultured and released individuals. Fish Res 77:159–172CrossRefGoogle Scholar
  94. Utter F (1998) Genetic problems of hatchery-reared progeny released into the wild, and how to deal with them. Bull Mar Sci 62:623–640Google Scholar
  95. Via S (2009) Natural selection in action during speciation. Proc Natl Acad Sci 106:9939–9946PubMedCrossRefGoogle Scholar
  96. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Gen 7:167–184CrossRefGoogle Scholar
  97. Waples RS, Do C (1994) Genetic risk associated with supplementation of Pacific salmonids: captive broodstock programs. Can J Fish Aquat Sci 51(S1):310–329CrossRefGoogle Scholar
  98. Waples RS, Do C (2008) L d N e: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756CrossRefGoogle Scholar
  99. Waples RS, Naish KA (2009) Genetic and evolutionary considerations in fishery management: research needs for the future. In: Beamish J, Rothschild BJ (eds) The future of fisheries science in North America. Springer, Dordrecht, pp 427–451CrossRefGoogle Scholar
  100. Waples RS, Hindar K, Hard JJ (2012) Genetic risks associated with marine aquaculture. NOAA Technical Memorandum NMFS-NWFSC-119. US Department of Commerce NOAA NMFS, Washington, DCGoogle Scholar
  101. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  102. Willing E-M, Dreyer C, van Oosterhout C (2012) Estimates of genetic differentiation measured by FST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7:e42649. doi: 10.1371/journal.pone.0042649 PubMedCentralPubMedCrossRefGoogle Scholar
  103. Withler RE, Campbell A, Li S, Miller KM, Brouwer D, Lucas BG (2001) High levels of genetic variation in northern abalone Haliotis kamtschatkana of British Columbia. Can Sci Adv Sec (CSAS) Res Doc 2001/097. CSAS, Ottowa, ONGoogle Scholar
  104. Withler RE, Campbell A, Li SR, Brouwer D, Supernault KJ, Miller KM (2003) Implications of high levels of genetic diversity and weak population structure for the rebuilding of northern abalone in British Columbia, Canada. J Shellfish Res 22:839–847Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • K. M. Gruenthal
    • 1
    • 10
  • D. A. Witting
    • 2
  • T. Ford
    • 3
  • M. J. Neuman
    • 4
  • J. P. Williams
    • 5
  • D. J. PondellaII
    • 5
  • A. Bird
    • 6
  • N. Caruso
    • 7
  • J. R. Hyde
    • 8
  • L. W. Seeb
    • 9
  • W. A. Larson
    • 9
  1. 1.Hubbs-SeaWorld Research InstituteSan DiegoUSA
  2. 2.Restoration Center, Office of Habitat Conservation, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationLong BeachUSA
  3. 3.Santa Monica Bay Restoration FoundationLos AngelesUSA
  4. 4.Protected Resources Division, Southwest Regional Office, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationLong BeachUSA
  5. 5.Vantuna Research Group, Moore LaboratoryOccidental CollegeLos AngelesUSA
  6. 6.Orange County CoastkeeperCosta MesaUSA
  7. 7.Get Inspired!, Inc.Garden GroveUSA
  8. 8.Fisheries Resources Division, Southwest Fisheries Science Center, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationLa JollaUSA
  9. 9.School of Aquatic and Fisheries SciencesUniversity of WashingtonSeattleUSA
  10. 10.Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationSeattleUSA

Personalised recommendations