Advertisement

Conservation Genetics

, Volume 7, Issue 5, pp 717–734 | Cite as

A genetic test for recruitment enhancement in Chesapeake Bay oysters, Crassostrea virginica, after population supplementation with a disease tolerant strain

  • Matthew P. HareEmail author
  • Standish K. AllenJr.
  • Paulette Bloomer
  • Mark D. Camara
  • Ryan B. Carnegie
  • Jenna Murfree
  • Mark Luckenbach
  • Donald Meritt
  • Cheryl Morrison
  • Kennedy Paynter
  • Kimberly S. Reece
  • Colin G. Rose
Article

Abstract

Many of the methods currently employed to restore Chesapeake Bay populations of the eastern oyster, Crassostrea virginica, assume closed recruitment in certain sub-estuaries despite planktonic larval durations of 2–3 weeks. In addition, to combat parasitic disease, artificially selected disease tolerant oyster strains are being used for population supplementation. It has been impossible to fully evaluate these unconventional tactics because offspring from wild and selected broodstock are phenotypically indistinguishable. This study provides the first direct measurement of oyster recruitment enhancement by using genetic assignment tests to discriminate locally produced progeny of a selected oyster strain from progeny of wild parents. Artificially selected oysters (DEBY strain) were planted on a single reef in each of two Chesapeake Bay tributaries in 2002, but only in the Great Wicomico River (GWR) were they large enough to potentially reproduce the same year. Assignment tests based on eight microsatellite loci and mitochondrial DNA markers were applied to 1579 juvenile oysters collected throughout the GWR during the summer of 2002. Only one juvenile oyster was positively identified as an offspring of the 0.75 million DEBY oysters that were planted in the GWR, but 153 individuals (9.7%) had DEBY ×wild F1 multilocus genotypes. Because oyster recruitment was high across the region in 2002, the proportionately low enhancement measured in the GWR would not otherwise have been recognized. Possible causes for low enhancement success are discussed, each bearing on untested assumptions underlying the restoration methods, and all arguing for more intensive evaluation of each component of the restoration strategy.

Keywords

assignment test Great Wicomico River F1 hybrid population enhancement restoration 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We are indebted to the cooperative efforts of several oyster restoration organizations and individuals that facilitated this research. In Maryland, construction of the artificial oyster reef and planting of DEBY oysters was done by the Oyster Recovery Partnership at the direction of Charlie Frentz. We␣appreciate help with spat collections by Cori Milbury, Stephanie Tobash, Horn Point hatchery interns and the Hare lab. In Virginia, coordination with restoration activities was achieved with the help of Rob Brumbaugh and Tommy Leggett of the Chesapeake Bay Foundation who oversaw nursery culture and planting of DEBYs in the GWR. We thank P.G. Ross, Jr., Alan Birch, Joshua Smith, Julie Stubbs and Gail Scott for help with spat collection and processing. Helpful comments have been provided by H. Wang, R. Mann, J. Harding, M. Southworth, W. Delport and members of the Hare lab. This work was funded by the Oyster Disease Research Program of NOAA/Sea Grant. VIMS contribution 2710.

References

  1. Allen SK, Brumbaugh RD, Schulte D (2003) Terraforming Chesapeake Bay. Virginia Marine Res. Bull. 35: 2–8Google Scholar
  2. Baker P, Mann R (2003) Late stage bivalve larvae in a well-mixed estuary are not inert particles. Estuaries 26: 837–845CrossRefGoogle Scholar
  3. Banks MA, Eichert W, Olsen JB (2003) Which genetic loci have greater population assignment power?. Bioinformatics, 19: 1436–1438PubMedCrossRefGoogle Scholar
  4. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) GENETIX 4.02, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions CNRS UMR 5000, Université de Montpellier II, Montpellier (France)Google Scholar
  5. Bernatchez L, Duchesne P (2000) Individual-based genotype analysis in studies of parentage and population assignment: how many loci, how many alleles? Can. J. Fish. Aquat. Sci. 57: 1–12CrossRefGoogle Scholar
  6. Bierne N, Launey S, Naciri-Graven Y, Bonhomme F (1998) Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics 148: 1893–1906PubMedGoogle Scholar
  7. Boesch D, Burreson E, Dennison W, et al. (2001) Factors in the decline of coastal ecosystems. Science 293: 1589–1590PubMedCrossRefGoogle Scholar
  8. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q. Rev. Biol. 74: 21–45PubMedCrossRefGoogle Scholar
  9. Brown BL, Franklin DE, Gaffney P, et al. (2000) Characterization of microsatellite loci in the eastern oyster, Crassostrea virginica. Mol. Ecol. 9: 2155–2234CrossRefGoogle Scholar
  10. Brumbaugh RD, Sorabella LA, Garcia CO, Goldsborough WJ, Wesson JA (2000) Making a case for community-based oyster restoration: an example from Hampton Roads, Virginia, USA. J. Shellfish Res. 19: 467–472Google Scholar
  11. Burreson EM, Ragone Calvo L (1996) Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. J. Shellfish Res. 15: 17–34Google Scholar
  12. Campbell D, Duchesne P, Bernatchez L (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Mol. Ecol. 12: 1979–1991PubMedCrossRefGoogle Scholar
  13. 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: 1989–2000PubMedGoogle Scholar
  14. Cox C, Mann R (1992) Temporal and spatial changes in fecundity of eastern oysters, Crassostrea virginica (Gmelin, 1791) in the James River, Virginia. J. Shellfish Res. 11: 49–54Google Scholar
  15. Davies N, Villablanca FX, Roderick GK (1999) Determining the source of individuals: multilocus genotyping in nonequilibrium population genetics. Trends. Ecol. Evol. 14q: 17–21CrossRefGoogle Scholar
  16. Estoup A, Largiader CR, Cornuet J-M, et al. (2000) Juxtaposed microsatellite systems as diagnostic markers for admixture: an empirical evaluation with brown trout (Salmo trutta) as model organism. Mol. Ecol. 9: 1873–1886PubMedCrossRefGoogle Scholar
  17. 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
  18. Galtsoff P (1938) Physiology of reproduction of Ostrea virginica II. Simulation of spawning in the female oyster. Biol. Bull. 75: 286–307Google Scholar
  19. Goudet J (2001) FSTAT, A Program to Estimate and Test Gene Diversities and Fixation Indices (version 2.9.3). Institut de Zoologie et d’Ecologie Animale, Universite de Lausane, LucerneGoogle Scholar
  20. Guinand B, Scribner KT, Topchy A, Page KS, Punch W, Burnham-Curtis MK (2004) Sampling issues affecting accuracy of likelihood-based classification using genetical data. Environ. Biol. Fishes 69: 245–259CrossRefGoogle Scholar
  21. Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite markers: methods and applications. Fish Fisher. 2: 93–112CrossRefGoogle Scholar
  22. Hare MP, Avise JC (1996) Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50: 2305–2315CrossRefGoogle Scholar
  23. Hilbish TJ (1996) Population genetics of marine species: the interaction of natural selection and historically differentiated populations. J. Exp. Mar. Biol. Ecol. 200: 67–83CrossRefGoogle Scholar
  24. Jackson JBC, Kirby MX, Berger WH, et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–638PubMedCrossRefGoogle Scholar
  25. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402: 802–804CrossRefGoogle Scholar
  26. Kennedy V (1996) Biology of larvae and spat. In: The Eastern oyster Crassostrea virginica (eds. Kennedy V, Newell RIE, Eble AF), p. 734. Maryland Sea Grant, College Park.Google Scholar
  27. Kinlan BP, Gaines S (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84: 2007–2020Google Scholar
  28. Launey S, Hedgecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159: 255–265PubMedGoogle Scholar
  29. Luckenbach M, Mann R, Wesson JE (1999) Oyster Reef Habitat Restoration: A Synopsis of Approaches, p. 366. Virginia Institute of Marine Science, Gloucester Point, VA.Google Scholar
  30. Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends. Ecol. Evol. 20: 136–142PubMedCrossRefGoogle Scholar
  31. Mann R (2000) Restoring the oyster reef communities in the Chesapeake Bay: A commentary. J. Shellfish Res. 19: 335–339Google Scholar
  32. Milbury CA (2003) Using mitochondrial DNA markers to monitor oyster stock enhancement in the Choptank River, Chesapeake Bay. MS thesis, University of DelawareGoogle Scholar
  33. Milbury CA, Meritt DW, Newell RIE, Gaffney PM (2004) Mitochondrial DNA markers allow monitoring of oyster stock enhancement in the Chesapeake Bay. Mar. Biol. 145: 351–359CrossRefGoogle Scholar
  34. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York, pp. 164–165Google Scholar
  35. Neigel JE (1997) A comparison of alternative strategies for estimating gene flow from genetic markers. Annu. Rev. Ecol. Syst. 28: 105–128CrossRefGoogle Scholar
  36. Paetkau D, Shields GF, Strobeck C (1998) Gene flow between insular, coastal and interior populations of brown bears in Alaska. Mol. Ecol. 7: 1283–1292PubMedCrossRefGoogle Scholar
  37. 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: 55–65PubMedCrossRefGoogle Scholar
  38. Palumbi S (1996) Macrospatial genetic structure and speciation in marine taxa with high dispersal abilities. In: Ferraris J, Palumbi S (eds), Molecular Zoology: Advances, Strategies, and Protocol. Wiley, New York, pp. 101–117Google Scholar
  39. Piry S, Alapetite A, Cornuet J-M, et al. (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95: 536–539PubMedCrossRefGoogle Scholar
  40. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959PubMedGoogle Scholar
  41. Ragone Calvo L, Burreson EM (2003) Status of the major oyster diseases in Virginia—2002. A summary of the annual monitoring program. In: Virginia Institute of Marine Science Marine Resource Reports. Virginia Institute of Marine Science, Gloucester Point, Virginia.Google Scholar
  42. Ragone Calvo L, Calvo GW, Burreson EM (2003) Dual disease resistance in a selectively bred eastern oyster, Crassostrea virginica, strain tested in Chesapeake Bay. Aquaculture 220: 69–87CrossRefGoogle Scholar
  43. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA 94: 9197–9201PubMedCrossRefGoogle Scholar
  44. Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124: 397–406PubMedGoogle Scholar
  45. Reece KS, Ribeiro WL, Gaffney PM, Carnegie RB, Allen SK (2004) Microsatellite marker development and analysis in the eastern oyster (Crassostrea virginica): confirmation of null alleles and non-Mendelian segregation ratios. J. Hered. 95: 346–352PubMedCrossRefGoogle Scholar
  46. Roques S, Duchesne P, Bernatchez L (1999) Potential of microsatellites for individual assignment: the North Atlantic redfish (genus Sebastes) species complex as a case study. Mol. Ecol. 8: 1703–1717PubMedCrossRefGoogle Scholar
  47. Rose CG, Paynter KT, Hare MP (2006) Isolation by distance in the eastern oyster, Crassostrea virginica, in Chesapeake Bay. J. Hered.Google Scholar
  48. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol. Appl. 13: S159–S169Google Scholar
  49. Siegel DA, Kinlan BP, Gaylord B, Gaines SD (2003) Lagrangian descriptions of marine larval dispersal. Mar. Ecol. Prog. Ser. 260: 83–96Google Scholar
  50. Southworth M, Harding JM, Mann R (2004) The Status of Virginia’s Public Oyster Resource 2003, p.55. Virginia Institute of Marine Science, Gloucester Point, VA.Google Scholar
  51. Southworth M, Mann R (1998) Oyster reef broodstock enhancement in the Great Wicomico River, Virginia. J. Shellfish Res. 17: 1101–1114Google Scholar
  52. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402: 799–802CrossRefGoogle Scholar
  53. Thompson R, Newell R, Kennedy V, Mann R (1996) Reproductive processes and early development. In: Kennedy V, Newell RIE, Eble AF (eds), The Eastern Oyster Crassostrea virginica. Maryland Sea Grant, College Park, pp. 335–370Google Scholar
  54. Thorrold SR, Jones GP, Hellberg ME, et al. (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull. Mar. Sci. 70: 291–308Google Scholar
  55. Thorrold SR, Latkoczy C, Swart PK, Jones CM (2001) Natal homing in a marine fish metapopulation. Science 291: 297–299PubMedCrossRefGoogle Scholar
  56. U.S. Army Corps of Engineers (2003) Final Decision Document Amendment Section 704(b) as Amended, Chesapeake Bay oyster Recovery Phase III, Great Wicomico River, Virginia, p. 117. U.S. Army Corps of Engineers, Norfolk District, Norfolk, VAGoogle Scholar
  57. Wang JL, Ryman N (2001) Genetic effects of multiple generations of supportive breeding. Conserv. Biol. 15: 1619–1631CrossRefGoogle Scholar
  58. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J. Hered. 89: 438–450CrossRefGoogle Scholar
  59. Waples RS, Do C (1994) Genetic risk associated with supplementation of Pacific Salmonids: captive broodstock programs. Can. J. Fish. Aquat. Sci. 51: 310–329Google Scholar
  60. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370CrossRefGoogle Scholar
  61. Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: Fst ≠ 1/(4Nm+1). Heredity 82: 117–125PubMedCrossRefGoogle Scholar
  62. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177–1191PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Matthew P. Hare
    • 1
    Email author
  • Standish K. AllenJr.
    • 2
  • Paulette Bloomer
    • 1
    • 3
  • Mark D. Camara
    • 2
    • 4
  • Ryan B. Carnegie
    • 2
  • Jenna Murfree
    • 1
  • Mark Luckenbach
    • 5
  • Donald Meritt
    • 6
  • Cheryl Morrison
    • 2
    • 7
  • Kennedy Paynter
    • 1
  • Kimberly S. Reece
    • 2
  • Colin G. Rose
    • 1
  1. 1.Biology DepartmentUniversity of MarylandCollege ParkUSA
  2. 2.Virginia Institute of Marine Science, College of William and MaryGloucester PointUSA
  3. 3.Molecular Ecology and Evolution Programme, Department of GeneticsUniversity of PretoriaPretoriaSouth Africa
  4. 4.Hatfield Marine Science CenterOregon State UniversityNewportUSA
  5. 5.Eastern Shore LaboratoryVirginia Institute of Marine Science, College of William and MaryWachapreagueUSA
  6. 6.Horn Point LaboratoryUniversity of Maryland Center for Environmental ScienceCambridgeUSA
  7. 7.US Geological Survey, Biological Resources DivisionLeetown Science Center, Aquatic Ecology BranchKearneysvilleUSA

Personalised recommendations