Genetic diversity and effective size of Atlantic sturgeon, Acipenser oxyrhinchus oxyrhinchus river spawning populations estimated from the microsatellite genotypes of marine-captured juveniles

Abstract

Juvenile Atlantic sturgeon (Acipenser oxyrhinchus oxyrhinchus) forming aggregations at coastal sites in the mid-Atlantic Bight were subjected to a mixed stock analysis (MSA) and individual-based assignment using twelve microsatellite loci. We confirmed earlier findings from an analysis of mitochondrial DNA that three river spawning populations (Hudson, James and Delaware Rivers) are the primary sources of these particular marine aggregations. Of the 460 individuals sampled 322, 36 and 47 were assigned to the Hudson, James and Delaware Rivers, respectively. MSA estimated that the New York Bight Distinct Population Segment (Hudson River and Delaware River) contributed 83–90 % of individuals to the marine aggregations and the Chesapeake (James River) and Southeast Distinct Population Segments contributed 5.5–11 %. Mean M-ratios were lower than expected at equilibrium in all three rivers (Delaware = 0.726, Hudson = 0.748, James = 0.664), indicative of genetic bottlenecks affecting all three spawning populations. Further, there were low but detectable levels of inbreeding in all three rivers populations. Effective population size (Ne) was estimated for three populations: Hudson River (172–230 individuals), James River (40–100 individuals) and Delaware River (75–186 individuals). Despite these issues, simulations based on life-history information and the Ne estimates suggest that if ongoing management measures are effective, contemporary levels of population genetic diversity are likely to be retained over the next century.

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References

  1. ASSRT (2007) Status review of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus). Report to the National Marine Fisheries Service, Northeast Regional Office. 23 Feb 2007 p 174

  2. Balazik MT, Garman GC, Fine ML, Hager CH, McIninch SP (2010) Changes in age composition and growth characteristics of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) over 400 years. Biol Lett 6:708–710

    PubMed  Article  PubMed Central  Google Scholar 

  3. Boreman J (1997) Sensitivity of North American sturgeons and paddlefish to fishing mortality. Environ Biol Fish 48:399–405

    Article  Google Scholar 

  4. Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462

    PubMed  Article  CAS  Google Scholar 

  5. Chapman DD, Simpfendorfer CA, Wiley TR, Poulakis GR, Curtis C, Tringali M, Carlson JK, Feldheim KA (2011) Genetic diversity despite population collapse in a critically endangered marine fish: the smalltooth sawfish (Pristis pectinata). J Hered 102:643–652

    PubMed  Article  Google Scholar 

  6. DeHaan PW, Libants SV, Elliot RF, Scribner KT (2006) Genetic population structure of remnant Lake sturgeon populations in the Upper Great Lakes Basin. Trans Am Fish Soc 135:1478–1492

    Article  CAS  Google Scholar 

  7. Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high levels of genetic variation. Conserv Biol 4:417–422

    Article  Google Scholar 

  8. Dunton KJ, Jordaan A, McKown KA, Conover DO, Frisk MG (2010) Abundance and distribution of Atlantic sturgeon (Acipenser oxyrinchus) within the North Atlantic Ocean, determined from five fishery-independent surveys. Fish B-NOAA 108

  9. Dunton KJ, Chapman DD, Jordaan A, Feldheim KA, O’Leary SJ, McKnown KA, Frisk MG (2012) Genetic mixed-stock analysis of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus in a heavily exploited marine habitat indicates the need for routine genetic monitoring. J Fish Biol 80:207–217

    PubMed  Article  CAS  Google Scholar 

  10. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  11. Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  12. Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–73

    Article  Google Scholar 

  13. Frasier TR (2008) STORM: software for testing hypotheses of relatedness and mating patterns. Mol Ecol Res 8:1263–1266

    Article  Google Scholar 

  14. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    PubMed  Article  CAS  Google Scholar 

  15. Gilbert CR (1989) Species Profiles. Life histories and environmental requirements of coastal fishes and invertebrates (Mid-Atlantic). Atlantic and Shortnose sturgeons. Florida University, Gainesville Florida Museum of Natural History

  16. Goudet J (1995) Fstat version 1.2: a computer program to calcluate F-statistics. J Hered 86:485–486

    Google Scholar 

  17. Grogan CS, Boreman J (1998) Estimating the probability that historical populations of fish species are extirpated. N Am J Fish Manag 18:522–529

    Article  Google Scholar 

  18. Grunwald C, Maceda L, Waldman J, Stabile J, Wirgin I (2008) Conservation of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus: delineation of stock structure and distinct population segments. Conserv Genet 9:1111–1124

    Article  Google Scholar 

  19. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P, Koren C, Nygard T, Volke V, Vila C, Ellegren H (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319

    PubMed  Article  PubMed Central  Google Scholar 

  20. 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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  21. Henderson-Arzapalo A, King TL (2002) Novel microsatellite markers for Atlantic sturgeon (Acipenser oxyrinchus) population delineation and broodstock management. Mol Ecol 2:437–439

    Article  CAS  Google Scholar 

  22. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  23. Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HK, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc Roy Soc B 272:497–503

    Article  Google Scholar 

  24. Kahnle AW, Hatalla KA, McKown KA (2007) Status of Atlantic sturgeon of the Hudson River Estuary, New York, USA. Am Fisher Soc Symp 56:347

    Google Scholar 

  25. Kalinowski ST, Manlove KR, Taper ML (2008) Oncor: a computer program for genetic stock identification, vol 2. Montana State University, Bozeman

    Google Scholar 

  26. King TL, Lubinski BA, Spidle AP (2001) Microsatellite DNA variation in Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) and cross-species amplification in the Acipenseridae. Conserv Genet 2:103–119

    Article  CAS  Google Scholar 

  27. Kuo C-H, Janzen FJ (2003) Bottlesim: a bottleneck simulation program for long-lived species with overlapping generations. Mol Ecol Notes 3:669–673

    Article  CAS  Google Scholar 

  28. Kuo C-H, Janzen FJ (2004) Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conserv Genet 5:425–437

    Article  CAS  Google Scholar 

  29. Lerner HRL, Johson JA, Lindsay AR, Kiff LF, Mindell DP (2009) It’s not too late for the harpy eagle (Harpia haryja): high levels of genetic diversity and differentiation can fuel conservation programs. PLoS ONE 4:e7336

    PubMed  Article  PubMed Central  Google Scholar 

  30. Lippé C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catastomidae, Pisces): the positive sides of a long generation time. Mol Ecol 15:1769–1780

    PubMed  Article  Google Scholar 

  31. Lynch M, Lande R (1998) The critical effective size for a genetically secure population. Anim Conserv 1:70–72

    Article  Google Scholar 

  32. Magnin E (1964) Croissance en longueur de trois esturgeons d’Amérique du Nord: Acipenser oxyrhynchus Mitchill, Acipenser fulvescens Raffinesque, et Acipenser brevirostris. Le Sueur. Int Ver für Theor und Angew Limnol Verh 15:968–974

    Google Scholar 

  33. Mesquita N, Hänfling B, Carvalho GR, Coelho MM (2005) Phylogeography of the cyprinid Squalius aradensis and implications for conservation of the endemic freshwater fauna of southern Portugal. Mol Ecol 14:1939–1954

    PubMed  Article  CAS  Google Scholar 

  34. Mourier J, Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Mol Ecol 22:201–214

    PubMed  Article  Google Scholar 

  35. Moyer GR, Sweka JA, Peterson DL (2012) Past and present processes influencing genetic diversity and effective population size in a natural population of Atlantic sturgeon. Trans Am Fish Soc 141:56–67

    Article  Google Scholar 

  36. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  PubMed Central  Google Scholar 

  37. NMFS (2010) Endangered and threatened wildlife; notice of 90-day finding on a petition to list Atlantic Sturgeon as threatened or endangered under the Endangered Species Act (ESA). Fed Reg 75:838–841

    Google Scholar 

  38. Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341

    Article  Google Scholar 

  39. O’Leary SJ, Hice LA, Feldheim KA, Frisk MG, McElroy AE, Fast MD, Chapman DD (2013) Severe inbreeding and small effective number of breeders in a formerly abundant marine fish. PLoS ONE 8:e66126

    PubMed  Article  PubMed Central  Google Scholar 

  40. Ong T-L, Stabile J, Wirgin I, Waldman JR (1996) Genetic divergence between Acipenser oxyrinchus oxyrinchus and A. o. desotoi as assessed by mitochondrial sequencing analysis. Copeia 1996:464–469

    Article  Google Scholar 

  41. Peterson DL, Schueller P, DeVries R, Fleming J, Grunwald C, Wirgin I (2008) Annual run size and genetic characteristics of Atlantic sturgeon in the Altamaha River, Georgia. Trans Am Fish Soc 137:393–401

    Article  Google Scholar 

  42. Piry S, Luikart G, Cornuet JM (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  43. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Heredity 86:248–249

    Google Scholar 

  44. Raymond M, Vaanto RL, Thomas F, Rousset F, de Meeus T, Renaud F (1997) Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Mar Ecol Prog Ser 156:225–237

    Article  Google Scholar 

  45. Secor DH (2002) Atlantic sturgeon fisheries and stock abundances during the late nineteenth century. Am Fish Soc Symp 28:89–98

    Google Scholar 

  46. Secor DH, Waldman JR (1999) Historical abundance of Delware Bay Atlantic sturgeon and potential rate of recovery. Am Fish Soc Symp 23:203–216

    Google Scholar 

  47. Smith TIJ, Clugston JP (1997) Status and management of Atlantic sturgeon, Acipenser oxyrinchus, in North America. Environ Biol Fish 48:335–346

    Article  Google Scholar 

  48. Stein AB, Friedland KB, Sutherland M (2004) Atlantic sturgeon marine distribution and habitat use along the Northeastern Coast of the United States. Trans Am Fish Soc 133:527–537

    Article  Google Scholar 

  49. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  50. Van Eenennaam JP, Doroshov SI, Moberg GP, Watson JG, Moore DS, Linares J (1996) Reproductive conditions of the Atlantic sturgeon (Acipenser oxyrinchus) in the Hudson River. Estuaries 19:769–777

    Article  Google Scholar 

  51. Waldman JR, Wirgin II (1998) Status and restoration options for Atlantic sturgeon in North America. Conser Biol 12:631–638

    Article  Google Scholar 

  52. Waldman JR, Hart JT, Wirgin I (1996) Stock composition of the New York Bight Atlantic sturgeon fishery based on analysis of mitochondrial DNA. Trans Am Fish Soc 125:364–371

    Article  CAS  Google Scholar 

  53. Waldman JR, King TL, Savoy T, Maceda L, Grunwald C, Wirgin I (2012) Stock origins of subadult and adult Atlantic Sturgeon, Acipenser oxyrinchus, in a non-natal estuary. Estuar Coast, Long Island Sound. doi:10.1007/s12237-012-9573-0

    Google Scholar 

  54. Wang S, Hard JJ, Utter F (2001) Salmonid inbreeding: a review. Rev Fish Biol Fisher 11:301–319

    Article  Google Scholar 

  55. Waples RS, Do C (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

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

    PubMed Central  Google Scholar 

  57. Waples RS, Luikart G, Faulkner JR, Tallmon DA (2013) Simple life-history traits explain key effective population size ratios across diverse taxa. Proc Roy Soc B 280:20131339

    Article  Google Scholar 

  58. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  59. Wirgin I, Waldman JR, Rosko J, Gross R, Collins MR, Rogers SG, Stabile J (2000) Genetic structure of Atlantic Sturgeon populations based on mitochondrial DNA control region sequences. Trans Am Fish Soc 129:476–486

    Article  CAS  Google Scholar 

  60. Wirgin I, Waldman JR, Stabile J, Lubinski B, King T (2002) Comparison of mitochondrial DNA control region sequence and microsatellite DNA analysis in estimating population structure and gene flow rates in Atlantic sturgeon Acipenser oxyrinchus. J Appl Ichtyol 18:313–319

    Article  CAS  Google Scholar 

  61. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

Funding for this study was provided by National Oceanic and Atmospheric Administration Office of Protected Resources Proactive Species Grants Program (NOAA Award NA10NMF4720039), US Fish and Wildlife Service State Wildlife Grant through the New York Department of Environmental Conservation (NYDEC). K. Dunton was also funded under the Hudson River Foundation Graduate Fellowship Program (award 55359). We thank project collaborators Kim McKown of the NYDEC and Adrian Jordaan of the University of Massachusetts Amherst. Additionally, we thank M. Wiggins, S. Cluett, and rest of R.V. Seawolf for assistance in collection of samples and graduate students Chris Martinez and Josh Zacharias for assistance in the field.

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Correspondence to Shannon J. O’Leary.

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O’Leary, S.J., Dunton, K.J., King, T.L. et al. Genetic diversity and effective size of Atlantic sturgeon, Acipenser oxyrhinchus oxyrhinchus river spawning populations estimated from the microsatellite genotypes of marine-captured juveniles. Conserv Genet 15, 1173–1181 (2014). https://doi.org/10.1007/s10592-014-0609-9

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Keywords

  • Bottleneck
  • Effective population size
  • Mixed-stock analysis
  • Individual-based assignment
  • Microsatellites