The Role of Genetics in Managing Declining Fisheries Resources
Main Article Content
Abstract
With increasing human population, rising consumer demand, and intensification of industrial fishing, many valued fisheries are in decline. This review and synthesis explores how genetics informs classical fisheries management programs, especially in the context of managing declining fisheries resources. Discussing underlying principles and illustrative case studies drawn as possible from Southeast Asia, I focus upon application of genetics to: (1) define biologically based management units, (2) monitor the impacts of fisheries and fishery management actions, and (3) guide and evaluate fisheries restoration activities. Because overexploitation and declining fisheries arise from issues of economics, sociology, and politics, an effective approach to their solution must itself be interdisciplinary; application of genetic principles provides a valuable addition to such a holistic fisheries management program. Increasingly, progressive fisheries management agencies have in-house capabilities for genetic assessment and monitoring functions. Against this background, developing countries might seek to build their capacity for applied population genetics, either within fisheries management agencies or via scientific collaboration with research-oriented universities. While much progress has been achieved, the task of applying genetics to the effective management of declining fisheries is large and mostly before us.
Article Details
References
2. Antoro, S., U. Na-Nakorn, and W Koedprang. 2006. Study of genetic diversity of orange-spotted grouper, Epinephelus coioides, from Thailand and Indonesia using microsatellite markers. Marine Biotechnology 8:17–26.
3. Appleyard, S.A., and R.D. Ward. 2006. Genetic diversity and effective population size in mass selection lines of Pacific oyster (Crassostrea gigas). Aquaculture 254:148-159.
4. Ayllon, F., J.L. Martinez, F. Juanes, S. Gephard and E. Garcia-Vazquez. 2006. Genetic history of the population of Atlantic salmon, Salmo salar L., under restoration in the Connecticut River, USA. ICES Journal of Marine Science 63:1286-1289.
5. Bartley, D., M. Bagley, G. Gall and B. Bentley. 1992. Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conservation Biology 6:365-375.
6. Beerli, P. and J. Felsenstein. 1999. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763-773.
7. Blankenship, H.L. and K.M. Leber. 1995. A responsible approach to marine stock enhancement. Pages 167-175 in H.L. Schramm, Jr. and R.G. Piper, eds. Uses and Effects of Cultured Fishes in Aquatic Ecosystems. American Fisheries Society Symposium, Bethesda, MD.
8. Busack, C.A. and K.P. Currens. 1995. Genetic risks and hazards in hatchery operations: fundamental concepts and issues. Pages 71-80 in H.L. Schramm and R.G. Piper, eds. Uses and Effects of Cultured Fishes in Aquatic Ecosystems. American Fisheries Society Symposium 15, Bethesda, MD.
9. Carey, C.S., J.W. Jones, R.S. Butler, and E.M. Hallerman. Restoring the endangered oyster mussel (Epioblasma capsaeformis) to the upper Clinch River, Virginia: an evaluation of population restoration techniques. Manuscript in review.
10. Chaney, M.L. and A.Y. Gracey. 2011. Mass mortality in Pacific oysters is associated with a specific gene expression signature. Molecular Ecology 20:2942-2954.
11. Cooke, S.J., S.G. Hinch, M.R. Donaldson, T.D. Clark, E.J. Eliason, G.T. Crossin, G.D. Raby, K.M. Jeffries, M. Lapointe, K. Miller, D.A. Patterson and A.P. Farrell. 2012. Conservation physiology in practice: how physiological knowledge has improved our ability to sustainably manage Pacific salmon during up-river migration. Philosophical Transactions of the Royal Society B 370:1757–1769.
12. Cornuet, J.-M. and G. Luikart. 1996. Description and power analysis of two tests for detecting recent demographic bottlenecks from allele frequency data. Genetics 144:2001-2014.
13. Crandall, K.A., D. Posada and D. Vasco. 1999. Effective population sizes: missing measures and missing concepts. Animal Conservation 2:317-319.
14. Dizon, A.E., C. Lockyear, W.F. Perrin, D.P. Demaster and J. Sisson. 1992. Rethinking the stock concept – a phylogeographic approach. Conservation Biology 6:24-36.
15. Do, C., R.S. Waples, D. Peel, G.M. Macbeth, B.J. Tillett and J.R. Ovenden. 2014. NeEstimator v2: re‐implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources 14:209-214.
16. Evans, T.G., F. Chan, B. A. Menge and G.E. Hofmann. 2013. Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment. Molecular Ecology 22:1609-1625.
17. Evans, T.G. and G.E. Hofmann. 2012. Defining the limits of physiological plasticity: how gene expression can assess and predict the consequences of ocean change. Philosophical Transactions of the Royal Society B 367:1733-1745.
18. Ewart, K.V., J.C. Belanger, J. Williams, T. Karakach, S. Penny, S.C.M. Tsoi, R.C. Richards and S.E. Douglas. 2005. Identification of gene differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Developmental and Comparative Immunology 29:333-347.
19. Faurby, S., T.L. King, M. Obst, E.M. Hallerman, C. Pertoldi, and P. Funch. 2010. Population dynamics of American horseshoe crabs – historic climatic events and recent anthropogenic pressures. Molecular Ecology 19:3088-3100.
20. Felsenstein, J. 1992. Estimating effective population size from samples of sequences: a bootstrap Monte Carlo integration method. Genetical Research 60:209-220.
21. Fu, Y.X. 1994a. A phylogenetic estimator of effective population size or mutation rate. Genetics 136:685-693.
22. Fu, Y.X. 1994b. Estimating effective population size or mutation rate using the frequencies of mutations of various classes in a sample of DNA sequences. Genetics 138:1375-1386.
23. Gaffney, P.M., V.P. Rubin, D. Hedgecock, D.A. Powers, G. Morris and L. Hereford. 1996. Genetic effects of artificial propagation: signals from wild and hatchery populations of red abalone in California. Aquaculture 143:257-266.
24. George, A.L., B.R. Kuhajda, J.D. Williams, M.A. Cantrell, P.L. Rakes and J.R. Shute. 2009. Guidelines for propagation and translocation for freshwater fish conservation. Fisheries 34:529-545.
25. Gustafson, R.G., T.C. Wainwright, G.A. Winans, F.W. Waknitz, L.T. Parker and R.S. Waples. 1997. Status review of sockeye salmon from Washington and Oregon. NOAA Technical Memorandum NMFS-NWFSC-33. http://www.nwfsc.noaa.gov/publications/scipubs/techmemos/tm33/int.html#wes.
26. Hastings, A. 1993. Complex interactions between dispersal and dynamics – lessons from coupled logistic equations. Ecology 74:1362–1372.
27. Hauser, L., G.J. Adcock, P.J. Smith, J.H. Bernal Ramírez and G.R. Carvalho. 2002. Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proceedings of the National Academy of Sciences U.S.A. 99:11742-11747.
28. Hedgecock, D., V. Chow and R.S. Waples. 1992. Effective population numbers of shellfish broodstocks estimated from temporal variance in allele frequencies. Aquaculture 108:215-232.
29. Hedgecock, D. and F.L. Sly. 1990. Genetic drift and effective population size of hatchery-propagated stocks of the Pacific oyster Crassostrea gigas. Aquaculture 88:21-38.
30. Hellberg, M.E., R.S. Burton, J.E. Neigel and S.R. Palumbi. 2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70(Suppl):273-290.
31. Hill, W.G. 1981. Estimation of effective population size from data on linkage disequilibrium. Genetical Research 38:209-216.
32. Hinch, S.G., S.J. Cooke, A.P. Farrell, K.M. Miller, M. Lapointe and D. A. Patterson. 2011. Dead fish swimming. Journal of Fish Biology 81:576-599.
33. Hoarau, G., E. Boon, D.N. Jongma, S. Ferber, J. Palsson, H.W. Van der Veer, A.D. Rijnsdorp, W.T. Stam and J.L. Olsen. 2005. Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proceedings of the Royal Society B: Biological Sciences 272:497-503.
34. Holling, C.S. (ed.). 1978. Adaptive Environmental Assessment and Management. John Wiley and Sons, Chichester, UK.
35. Jones, J., E. Hallerman and R. Neves. 2006. Genetic management guidelines for conservation and captive propagation of freshwater mussels. Journal of Shellfish Research 25:527-535.
36. Jorde, P.E. and N. Ryman. 1995. Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077-1090.
37. Ju, Z., M.C. Wells, S.J. Heater and R.B. Walter. 2007. Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia. Comparative Biochemistry and Physiology C – Toxicology and Pharmacology 145:134-144.
38. Klinbunga, S., P. Pripue, N. Khamnamtong, N. Puanglarp, A. Tassanakajon, P. Jarayaphand, I. Hirono, T. Aoki and P. Menasveta. 2003. Genetic diversity and molecular markers of the tropical abalone (Haliotis asinina) in Thailand. Marine Biotechnology 5:505-517.
39. Klinbunga, S., D. Siludjai, W. Wudthijinda, A. Tassanakajon, P. Jarayaphand and P. Menasveta. 2001. Genetic heterogeneity of the giant tiger prawn (Penaeus monodon) in Thailand revealed by RAPD and mitochondrial DNA RFLP analyses. Marine Biotechnology 3:428-438.
40. Koskinen, H., P. Pehkonen, E. Vehniane, A. Krasnov, C. Rexroad, S. Afanasyev, H. Molsa and A. Oikari. 2004. Response of rainbow trout transcriptome to model chemical contaminants. Biochemical and Biophysical Research Communications 320:745-753.
41. Krasnov, A., H. Koskinen, C. Rexroad, S. Afanasyev, H. Molsa and A. Oikari. 2005. Transcriptome responses to carbon tetrachloride and pyrene in the kidney and liver of juvenile rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 74:70-81.
42. Kuhner, M.K., J. Yamato and J. Felsenstein. 1995. Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. Genetics 140:1421-14300.
43. Laurie-Ahlberg, C. and B.S. Weir. 1979. Allozyme variation and linkage disequilibrium in some laboratory populations of Drosophila melanogaster. Genetical Research 32:215-229.
44. Letcher, B.H. and T.L. King. 1999. Targeted stock identification using multilocus genotype ‘familyprinting’. Fisheries Research 43:99-111.
45. Letcher, B.H. and T.L. King. 2001. Parentage and grandparentage assignment with known and unknown matings: application to Connecticut River Atlantic salmon restoration. Canadian Journal of Fisheries and Aquatic Sciences 58:1812-1821.
46. Lorenzen, K., K.M. Leber and H.L. Blankenship. 2010. Responsible approach to marine stock enhancement: an update. Reviews in Fisheries Science 18:189-210.
47. Luikart, G. and J.-M. Cornuet. 1999. Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211-1216.
48. Martinez, J.L., S. Gephard, F. Juanes and E. Garcia-Vazquez. 2001. Genetic and life history differentiation between donor and derivative populations of Atlantic salmon. Transactions of the American Fisheries Society 130:508-515.
49. McGoodwin, J.R. 1990. Crisis in the World’s Fisheries: People, Problems, and Policies. Stanford University Press, Stanford, CA.
50. Miller, K.M., S. Li, K.H. Kaukinen, N. Ginther, E. Hammill, J.M.R. Curtis, D.A. Patterson, T. Sierocinski, L. Donnison, P. Pavlidis, S.G. Hinch, K.A. Hruska, S.J. Cooke, K.K. English and A.P. Farrell. 2011. Genomic signatures predict migration and spawning failure in wild Canadian salmon. Science 331:214-217.
51. Miller, K.M., A. Teffer, S. Tucker, S. Li, A.D. Schulze, M. Trudel, F. Juanes, A. Tabata, K.H. Kaukinen, N.G. Ginther, T.J. Ming, S.J. Cooke, J.M. Hipfner, D.A. Patterson and S.G. Hinch. 2014. Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evolutionary Applications 7:812-855.
52. Miller, L.M., and A.R. Kapuscinski. 1997. Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 147:1249-1258.
53. Miller, L.M. and A.R. Kapuscinski. 2003. Genetic guidelines for hatchery supplementation programs. Pages 329-355 in E.M. Hallerman, ed. Population Genetics: Principles and Applications for Fisheries Scientists. American Fisheries Society, Bethesda, MD.
54. Moritz C., 1994. Defining ‘evolutionary significant units’ for conservation. Trends in Ecology and Evolution 9:373-375.
55. Na-Nakorn, U., M. Hara, N. Taniguchi, and S. Seki. 1998. Isozyme variation of Clarias macrocephalus from four locations in Thailand. Fisheries Science 64:526-530.
56. Na-Nakorn, U., P. Sodsuk, P. Wongrat, S. Janekitkarn and D.M. Bartley. 2002. Isozyme variation among four species of the catfish genus Clarias. Journal of Fish Biology 60:1051-1057.
57. Na-Nakorn, U., S. Sukmanomon, M. Nakajima, N. Taniguchi, W. Kamonrat, S. Poompuang and T. T. T. Nguyen. 2006. MtDNA diversity of the critically endangered Mekong giant catfish (Pangasianodon gigas Chevey, 1913) and closely related species: implications for conservation. Animal Conservation 9:483-494.
58. Na-Nakorn, U., N. Taniguchi, S. Seki, N. Estu and W. Kamonrat. 1999. Microsatellite loci from Thai walking catfish, Clarias macrocephalus and their application to population genetics study. Fisheries Science 65:520-526.
59. Nei, M. and F. Tajima. 1981. Genetic drift and estimation of effective population size. Genetics 98:625-640.
60. Ngamsiri, T., M. Nakajima, S. Sukmanomon, N. Sukumasavin, W. Kamonrat, U. Na-Nakorn and N. Taniguchi. 2007. Genetic diversity of wild Mekong giant catfish Pangasianodon gigas collected from Thailand and Cambodia. Fisheries Science 73:792–799.
61. Nielsen, R., J.L. Mountain, J.P. Huelsenbeck and M. Slatkin. 1998. Maximum likelihood estimation of population divergence times and population phylogeny in models without mutation. Evolution 52:660-677.
62. Olsen, J.B., P. Bentzen, M.A. Banks, J.B. Shaklee and S. Young. 2000. Microsatellites reveal population identity of individual pink salmon to allow supportive breeding of a population at risk of extinction. Transactions of the American Fisheries Society 129:323-242.
63. O'Leary, S.J., L.A. Hice, K.A. Feldheim, M.G. Frisk, A.E. McElroy, M.D. Fast and D.D. Chapman. 2013. Severe inbreeding and small effective number of breeders in a formerly abundant marine fish. PloS One 8(6):e66126.
64. O’Ryan, C., E.H. Harley, M.W. Bruford, M. Beaumon, R.K. Wayne and M.I. Cherry. 1998. Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Animal Conservation 1:85-94.
65. Palmer, G., J. Williams, M. Scott, E. Hallerman, K. Finne, N. Johnson, D. Dutton and B. Murphy. 2007. Genetic marker-assisted restoration of the presumptive native walleye stock in the upper New River, Virginia and West Virginia. Proceedings of the Southeastern Association of Fisheries and Wildlife Agencies 61:17-22.
66. Palsbøll P.J., M. Berube and F.W. Allendorf. 2007. Identification of management units using population genetic data. Trends in Ecology and Evolution 22:11-16.
67. Peatman, E. and Z. Liu. 2007. Microarray fundamentals: basic principles and applications in aquaculture. Pages 355-368 in Z. Liu (ed.). Aquaculture Genome Technologies. Blackwell Publishing, Oxford, UK.
68. Pollack, E. 1983. A new method for estimating the effective population size from allele frequency changes. Genetics 104:531-548.
69. Pudovkin, A.I., D.V. Zaykin and D. Hedgecock. 1996. On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383-387.
70. Ramstad, K.M., Woody C.A., Sage G.K. and F.W. Allendorf, 2004. Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska. Molecular Ecology 13:277–290.
71. Reiss, H., G. Hoarau, M. Dickey‐Collas and W.J. Wolff. 2009. Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish and Fisheries 10:361-395.
72. Rise, M.L., S.R.M. Jones, G.D. Brown, K.R. von Schalburg, W.S. Davidson and B.F. Koop. 2004. Microarray analyses identify molecular biomarkers of Atlantic salmon macrophage and hematopoietic kidney response to Piscirickettsia salmonis infection. Physiological Genomics 20:21-35.
73. Rise, M.L., K.R. von Schalburg, G.A. Cooper and B.F. Koop. 2007. Salmonid DNA microarrays and other tools for functional genomics research. Pages 369-411 in Z. Liu (ed.). Aquaculture Genome Technologies. Blackwell Publishing, Oxford, UK.
74. Ryder, O. 1986. Species conservation and systematics: the dilemma of subspecies. Trends in Ecology and Evolution 1:9-10.
75. Ryman, N. and L. Laikre. 1991. Effects of supportive breeding on the genetically effective population size. Conservation Biology 5:325-329.
76. Schwartz, M.K., D.A. Tallmon and G. Luikart. 1998. Review of DNA-based census and effective population size estimators. Animal Conservation 1:293-299.
77. Schwartz, M.K., D.A. Tallmon and G. Luikart. 1999. Using genetics to estimate the size of wild populations: many methods, much potential, uncertain utility. Animal Conservation 2:321-323.
78. Shaklee, J.B. and K.P. Currens. 2003. Genetic stock identification and risk assessment. Pages 291-328 in E. Hallerman (ed.). Population Genetics: Principles and Applications for Fisheries Scientists. American Fisheries Society, Bethesda, MD.
79. Shute, J.R., P.L. Rakes and P.W. Shute. 2005. Reintroduction of four imperiled fishes in Abrams Creek, Tennessee. Southeastern Naturalist 4:93-110.
80. Spidle, A.P., T.L. King and B.H. Letcher. 2004. Comparison of genetic diversity in the recently founded Connecticut River Atlantic salmon population to that of its primary donor stock, Maine's Penobscot River. Aquaculture 236:253-265.
81. Storz, J.F. and M.A. Beaumont. 2002. Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154-166.
82. Tajima, F. 1992. Statistical method for estimating the effective population size in Pacific salmon. Journal of Heredity 83:309-311.
83. Ton, C., D. Stamatiou, V.J. Dzau and C.C. Liew. 2002. Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development. Biochemical and Biophysical Research Communications 296:1134-1142.
84. UNFAO (Food and Agriculture Organization of the United Nations). 2014. The State of World Fisheries and Aquaculture 2014: Opportunities and Challenges. http://www.fao.org/3/a-i3720e/index.html. Accessed November 7, 2014.
85. U.S. Fish and Wildlife Service and National Marine Fisheries Service. 2000. Policy regarding controlled propagation of species listed under the Endangered Species Act. Federal Register 65:56916–56922.
86. Wang, J. 2005. Estimation of effective population sizes from data on genetic markers. Philosophical Transactions of the Royal Society B 360:1395-1409.
87. Waples, R.S. 1989. A generalized method for estimating population size from temporal changes in allele frequency. Genetics 121:379-191.
88. Waples, R.S. 1990. Conservation genetics of Pacific salmon. III. Estimating effective population size. Journal of Heredity 81:277-289.
89. Waples, R.S. 1991. Pacific salmon, Oncorynchus spp., and the definition of ‘species’ under the Endangered Species Act. Marine Fisheries Review 53:11-22.
90. Waples, R.S. and C. Do. 2010. Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolutionary Applications 3:244-262.
91. Waples, R.S. and D.J. Teel. 1990. Conservation genetics of Pacific salmon. I. Temporal changes in allele frequency. Conservation Biology 4:144-156.
92. Winans, G.A., D. Viele, A. Grover, M. Palmer-Zwahlen, D. Teel and D. Van Doornik. 2001. An update of genetic stock identification of Chinook salmon in the Pacific Northwest: Test fisheries in California. Reviews in Fisheries Science 9:213-237.
93. Zhang, J., W. Chu and G. Fu. 2009. DNA microarray technology and its application in fish biology and aquaculture. Frontiers in Biology China 4:305-313.