Interannual variation in effective number of breeders and estimation of effective population size in long-lived iteroparous lake sturgeon (Acipenser fulvescens)

Molecular Ecology

Volumn 22, Issue 5, 2013, Pages 1282-1294

  Duong, Thuy Yen ^a   Scribner, Kim T ^a   Forsythe, Patrick S ^a,c   Crossman, James A ^a,d   Baker, Edward A ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN DEPARTMENT OF NATURAL RESOURCES   (United States)

^c UNIVERSITY OF WISCONSIN GREEN BAY   (United States)

^d BC HYDRO   (Canada)

Author keywords

demographic parameters; effective number of breeders; effective population size; iteroparity; lake sturgeon; linkage disequilibrium

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ARTICLE; ECOLOGY; ECOSYSTEM; ENVIRONMENT; FEMALE; FISH; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC VARIABILITY; GENETICS; GENOTYPE; INBREEDING; LARVA; MALE; POPULATION DENSITY; POPULATION GENETICS; REPRODUCTION; RIVER; SEX RATIO;

ANIMALS; ECOLOGY; ECOSYSTEM; ENVIRONMENT; FEMALE; FISHES; GENETIC LOCI; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; INBREEDING; LARVA; LINKAGE DISEQUILIBRIUM; MALE; MICROSATELLITE REPEATS; POPULATION DENSITY; REPRODUCTION; RIVERS; SEX RATIO;

ACIPENSER FULVESCENS;

EID: 84874448094     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12167     Document Type: Article

References (88)

1. Araki H, Waples RS, Ardren WR, Cooper B, Blouin MS, (2007) Effective population size of steelhead trout: influence of variance in reproductive success, hatchery programs, and genetic compensation between life-history forms. Molecular Ecology, 16, 953-966.
2. Ardren WR, Kapuscinski AR, (2003) Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout. Molecular Ecology, 12, 35-49.
3. Auer NA, (1999) Population characteristics and movements of Lake Sturgeon in the Sturgeon River and Lake Superior. Journal of Great Lakes Research, 25, 282-293.
4. Baker EA, Borgeson DJ, (1999) Lake sturgeon abundance and harvest in Black Lake, Michigan, 1975-1999. North American Journal of Fisheries Management, 19, 1080-1088.
5. Barker JSF, (2011) Effective population size of natural populations of Drosophila buzzatii, with a comparative evaluation of nine methods of estimation. Molecular Ecology, 20, 4452-4471.
6. Bartley D, Bagley M, Gall G, Bentley B, (1992) Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conservation Biology, 6, 365-375.
7. Beebee TJC, (2009) A comparison of single-sample effective size estimators using empirical toad (Bufo calamita) population data: genetic compensation and population size-genetic diversity correlations. Molecular Ecology, 18, 4790-4797.
8. Birstein VJ, (1993) Sturgeons and paddlefishes: threatened fishes in need of conservation. Conservation Biology, 7, 773-787.
9. Bruch RM, Miller G, Hansen MJ, (2006) Fecundity of lake sturgeon (Acipenser fulvescens, Rafinesque) in Lake Winnebago, Wisconsin, USA. Journal of Applied Ichthyology, 22, 116-118.
10. Caballero A, (1994) Developments in the prediction of effective population size. Heredity, 73, 657-679.
11. Caroffino DC, Sutton TM, Elliott RF, Donofrio MC, (2010) Early life stage mortality rates of lake sturgeon in the Peshtigo River, Wisconsin. North American Journal of Fisheries Management, 30, 295-304.
12. Cervantes I, Goyache F, Molina A, Valera M, Gutiérrez JP, (2011) Estimation of effective population size from the rate of coancestry in pedigreed populations. Journal of Animal Breeding Genetics, 128, 56-63.
13. Charlesworth B, (2009) Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics, 10, 195-205.
14. Crossman J, Scribner KT, Duong TY, Davis C, Forsythe P, Baker E, (2011) Gamete and larval collection methods and hatchery rearing environments affect levels of genetic diversity in early life stages of lake sturgeon. Aquaculture, 310, 312-324.
15. Crow JF, Denniston C, (1988) Inbreeding and variance effective population numbers. Evolution, 42, 482-495.
16. Crow JF, Morton NE, (1955) Measurement of gene frequency drift in small populations. Evolution, 9, 202-214.
17. DeHaan PW, Libants SV, Elliott RF, Scribner KT, (2006) Genetic population structure of remnant lake sturgeon populations in the upper Great Lakes basin. Transactions of the American Fisheries Society, 135, 1478-1492.
18. Doctor KK, Quinn TP, (2009) Potential for adaptation-by-time in sockeye salmon (Oncorhynchus nerka): the interactions of body size and in-stream reproductive life span with date of arrival and breeding location. Canadian Journal of Zoology, 87, 708-717.
19. Duchesne P, Castric T, Bernatchez L, (2005) PASOS (parental allocation of singles in open systems): a computer program for individual parental allocation with missing parents. Molecular Ecology Notes, 5, 701-704.
20. Duong TY, (2010) Effects of spawning behavior and environmental factors on adult reproductive ecology and larval dispersal of lake sturgeon (Acipenser fulvescens). Ph.D. thesis, Department of Fisheries and Wildlife, Michigan State University, East Lansing, Michigan.
21. Duong TY, Scribner KT, Crossman J, Forsythe P, Baker E, (2011a) Environmental and maternal effects on embryonic and larval developmental time until dispersal of lake sturgeon (Acipenser fulvescens). Canadian Journal of Fisheries and Aquatic Sciences, 68, 643-654.
22. Duong TY, Scribner KT, Crossman J, et al,. (2011b) Relative larval loss among females during dispersal of lake sturgeon (Acipenser fulvescens). Environmental Biology of Fishes, 91, 459-469.
23. England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G, (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conservation Genetics, 7, 303-308.
24. Felsenstein J, (1971) Inbreeding and variance effective numbers in populations with overlapping generations. Genetics, 68, 581-597.
25. Forsythe PS, (2010) Evaluation of exogenous variables affecting spawning timing, natural egg deposition and mortality during the early life stages of lake sturgeon. Ph.D. thesis, Department of Zoology, Michigan State University, East Lansing, Michigan.
26. Forsythe P, Crossman J, Bello N, Baker E, Scribner KT, (2012a) Individual-basd analyses reveal high repeatability in timing and location of reproduction in lake sturgeon (Acipenser fulvescens). Canadian Journal of Fisheries and Aquatic Sciences, 69, 60-72.
27. Forsythe P, Scribner KT, Crossman J, et al,. (2012b) Environmental and lunar cues are predictive of the timing of river entry and spawning-site arrival in lake sturgeon Acipenser fulvescens. Journal of Fish Biology, 81, 35-53.
28. Frankham R, (1995) Effective population-size adult-population size ratios in wildlife-a Review. Genetical Research, 66, 95-107.
29. Gautschi B, Müller JP, Schmid B, Shykoff JA, (2003) Effective number of breeders and maintenance of genetic diversity in the captive bearded vulture population. Heredity, 91, 9-16.
30. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/ softwares/fstat.html. Updated from Goudet (1995).
31. Harkness WJK, Dymond JR, (1961) The Lake Sturgeon: the History of its Fishery and Problems of Conservation. Ontario Department of Lands and Forests, Ontario, 121 pp.
32. Hedgecock D, (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Genetics and Evolution of Aquatic Organisms (ed, Beaumont A,), pp. 122-134. Chapman and Hall, London.
33. Hedrick P, (2005) Large variance in reproductive success and the N-e/N ratio. Evolution, 59, 1596-1599.
34. Hendry AP, Day T, (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology, 14, 901-916.
35. Hill WG, (1972) Effective size of populations with overlapping generations. Theoretical Population Biology, 3, 278-289.
36. Hill WG, (1979) Note on effective population-size with overlapping generations. Genetics, 92, 317-322.
37. Hill WG, (1981) Estimation of effective population-size from data on linkage disequilibrium. Genetical Research, 38, 209-216.
38. Jorde PE, Ryman N, (1995) Temporal allele frequency change and estimation of effective size with overlapping generations. Genetics, 179, 1077-1090.
39. Kalinowski ST, Taper ML, Marshall TC, (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16, 1099-1106.
40. Kincaid H, (1999) Genetic considerations for captive breeding programs to preserve genetic variability. In: Workshop proceedings: Great Lakes Lake Sturgeon Genetics: Status, Needs, and Standardization. (ed, Lowie C,), pp. 4-5, Chicago, Illinois.
41. King TL, Lubinski BA, Spidle AP, (2001) Microsatellite DNA variation in Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) and cross-species amplification in the Acipenseridae. Conservation Genetics, 2, 103-119.
42. Lippe C, Dumont P, Bernatchez L, (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Molecular Ecology, 15, 1769-1780.
43. Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW, (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics, 11, 355-373.
44. Mackay TFC, (2007) Wild populations are smaller than we think: a commentary on 'Effective population size/adult population size ratios in wildlife: a review' by Richard Frankham. Genetics Research, 89, 489.
45. McQuown EC, Sloss BL, Sheehan RJ, Rodzen J, Tranah GJ, May B, (2000) Microsatellite analysis of genetic variation in sturgeon: new primer sequences for Scaphirhynchus and Acipenser. Transactions of the American Fisheries Society, 129, 1380-1388.
46. McQuown E, Gall GAE, May B, (2002) Characterization and inheritance of six microsatellite loci in lake sturgeon. Transactions of the American Fisheries Society, 131, 299-307.
47. Myers RA, (1998) When do environment-recruitment correlations work? Reviews in Fish Biology and Fisheries, 8, 285-305.
48. Nunney L, (1991) The influence of age structure and fecundity on effective population size. Proceedings of the Royal Society of London Series B-Biological Sciences, 246, 71-76.
49. Nunney L, (1993) The influence of mating system and overlapping generations on effective population size. Evolution, 47, 1329-1341.
50. Nunney L, (1996) The influence of variation in female fecundity on effective population size. Biological Journal of the Linnean Society, 59, 411-425.
51. Osborne MJ, Davenport SR, Hoagstrom CW, Turner TF, (2010) Genetic effective size, N-e, tracks density in a small freshwater cyprinid, Pecos bluntnose shiner (Notropis simus pecosensis). Molecular Ecology, 19, 2832-2844.
52. 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? Molecular Ecology, 17, 3428-3447.
53. Pearse DE, Anderson EC, (2009) Multiple paternity increases effective population size. Molecular Ecology, 18, 3124-3127.
54. Peel D, Ovenden JR, Peel SL, (2004) NeEstimator: Software for Estimating Effective Population Size, Version 1.3, Queensland Government, Department of Primary Industries and Fisheries, Brisbane, Australia.
55. Phillipsen IC, Bowerman J, Blouin M, (2010) Effective number of breeding adults in Oregon spotted frogs (Rana pretiosa): genetic estimates at two life stages. Conservation Genetics, 11, 737-745.
56. Phillipsen IC, Funk WC, Hoffman EA, Monsen KJ, Blouin MS, (2011) Comparative analyses of effective population size within and among species: Ranid frogs as a case study. Evolution, 65, 2927-2945.
57. Raymond M, Rousset F, (1995) Genepop (Version-1.2)-Population-genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
58. R-Development-Core-Team (2009) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
59. Robinson JD, Moyer GR, (2012) Linkage disequilibrium and effective population size when generations overlap. Evolutionary Applications, Early View.
60. Rochard E, Castelnaud G, Lepage M, (1990) Sturgeons (Pisces, Acipenseridae)-threats and prospects. Journal of Fish Biology, 37, 123-132.
61. Rousset F, (2008) GENEPOP '007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
62. Saarinen EV, Austin JD, Daniels JC, (2010) Genetic estimates of contemporary effective population size in an endangered butterfly indicate a possible role for genetic compensation. Evolutionary Applications, 3, 28-39.
63. Schwartz MK, Tallmon DA, Luikart G, (1998) Review of DNA-based census and effective population size estimators. Animal Conservation, 1, 293-299.
64. Schwartz MK, Luikart G, Waples RS, (2007) Genetic monitoring as a promising tool for conservation and management. Trends in Ecology and Evolution, 22, 25-33.
65. Serbezov D, Jorde PE, Bernatchez L, Olsen EM, Vøllestad LA, (2012a) Life history and demographic determinants of effective/census size ratios as exemplified by brown trout (Salmo trutta). Evolutionary Applications, 5, 607-618.
66. Serbezov D, Jorde PE, Bernatchez L, Olsen EM, Vøllestad LA, (2012b) Short-term genetic changes: evaluating effective population size estimates in a comprehensively described brown trout (Salmo trutta) population. Genetics, 191, 579-592.
67. Shrimpton JM, Heath DD, (2003) Census vs. effective population size in chinook salmon: large- and small-scale environmental perturbation effects. Molecular Ecology, 12, 2571-2583.
68. Smith KM, King DK, (2005) Dynamics and extent of larval lake sturgeon Acipenser fulvescens drift in the Upper Black River, Michigan. Journal of Applied Ichthyology, 21, 161-168.
69. Sugg DW, Chesser RK, (1994) Effective population sizes with multiple paternity. Genetics, 137, 1147-1155.
70. Tallmon DA, Koyuk A, Luikart G, Beaumont MA, (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Molecular Ecology Resources, 8, 299-301.
71. Tringali MD, Bert TM, (1998) Risk to genetic effective population size should be an important consideration in fish stock-enhancement programs. Bulletin of Marine Science, 62, 641-659.
72. 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.
73. Wang JL, (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Molecular Ecology, 18, 2148-2164.
74. Waples RS, (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics, 121, 379-391.
75. Waples RS, (1990) Conservation genetics of Pacific salmon. 2. Effective population size and the rate of loss of genetic variability. Journal of Heredity, 81, 267-276.
76. Waples RS, (1991) Genetic interactions between hatchery and wild salmonids-Lessons from the Pacific-Northwest. Canadian Journal of Fisheries and Aquatic Sciences, 48, 124-133.
77. Waples RS, (2002a) Effective size of fluctuating salmon populations. Genetics, 161, 783-791.
78. Waples RS, (2002b) Evaluating the effect of stage-specific survivorship on the N-e/N ratio. Molecular Ecology, 11, 1029-1037.
79. Waples RS, (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conservation Genetics, 7, 167-184.
80. Waples RS, (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Molecular Ecology Resources, 10, 785-796.
81. Waples RS, Do C, (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources, 8, 753-756.
82. Waples RS, Do C, (2010) Linkage disequilibrium estimates of contemporary N-e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolutionary Applications, 3, 244-262.
83. Waples RS, Waples RK, (2011) Inbreeding effective population size and parentage analysis without parents. Molecular Ecology Resources, 11 (Suppl. 1), 162-171.
84. Waples RS, Jensen DW, McClure M, (2010) Eco-evolutionary dynamics: fluctuations in population growth rate reduce effective population size in chinook salmon. Ecology, 91, 902-914.
85. Welsh AB, Blumberg M, May B, (2003) Identification of microsatellite loci in lake sturgeon, Acipenser fulvescens, and their variability in green sturgeon, A-medirostris. Molecular Ecology Notes, 3, 47-55.
86. Welsh AB, Elliott RF, Scribner KT, et al,. (2010) Genetic Guidelines for the Stocking of Lake Sturgeon (Acipenser fulvescens) in the Great Lakes Basin. Great Lakes Fishery Commission.
87. Winemiller KO, Rose KA, (1992) Patterns of life-history diversification in North American fishes: implications for population regulation. Canadian Journal of Fisheries and Aquatic Science, 49, 2196-2218.
88. Wright S, (1931) Evolution in Mendelian populations. Genetics, 16, 97-159.