Abstract
Once widely abundant, most subpopulations of the endangered Atlantic sturgeon are now estimated to be only 1–10% of their historical levels. The Edisto River has been sampled for a long period and extensively for juvenile Atlantic sturgeon from separate spring- and fall-spawned cohorts. Our objectives are to characterize the genetic diversity, stability, adaptive potential, and potential genetic structure of Atlantic sturgeon in the Edisto River and to identify any past bottlenecks experienced by this species, as well as to conduct forward simulation modeling of the population under multiple population trajectories. Our results indicate that fall- and spring-spawned Atlantic sturgeon in the Edisto River are genetically distinct (overall \({{F}_{ST}}\) = 0.092) with little gene flow or admixture between groups, both of which are diverse from a neutral genetic marker standpoint. Genetic diversity of both groups is on the higher end of published population diversity values. A lack of inbreeding and recent bottlenecks also bode well for these two groups of sturgeon, although future projections indicate a loss of allelic richness and genetic diversity even with population stability. Our effective population size estimates are moderate compared to published estimates for other Atlantic sturgeon populations. The most significant finding of our research is the genetic distinctness of the fall- and spring-spawned Atlantic sturgeon in the Edisto River, which may have several important ramifications for management of the species, including re-evaluating the demarcation of distinct population segments.
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References
Anders PJ, Drauch-Schreier A, Rodzen J, Powell MS, Narum S, Crossman JA (2011) A review of genetic evaluation tools for conservation and management of North American sturgeons: roles, benefits, and limitations. J Appl Ichthyol 27:3–11
Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program Structure. Mol Ecol Resour 8:1219–1229
ASSRT (2007) Status review of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus). Report to National Marine Fisheries Service, Northeast Regional Office Februrary, 23, 174.
Bain MB (1997) Atlantic and shortnose sturgeons of the Hudson River: common and divergent life history attributes. Sturgeon biodiversity and conservation. Springer, The Netherlands. pp. 347–358
Balazik MT, Musick JA (2015) Dual annual spawning races in Atlantic sturgeon. PloS ONE 10:e0128234. doi:10.0128210.0121371/journal.pone.0128234
Balazik MT, Garman GC, Van Eenennaam JP, Mohler J, Woods LC (2012) Empirical evidence of fall spawning by Atlantic sturgeon in the James River, Virginia. Trans Am Fish Soc 141:1465–1471
Banks MA, Rashbrook VK, Calavetta MJ, Dean CA, Hedgecock D (2000) Analysis of microsatellite DNA resolves genetic structure and diversity of chinook salmoon (Oncorhynchus tshawytscha) in California’s central valley. Can J Fish Aquat Sci 57:915–927
Beasley BR, Marshall WD, Miglarese AH, Scurry JD, Vanden Houten C (1996) Managing resources for a sustainable future: the Edisto River Basin Project report. South Carolina Department of Natural Resources, Columbia, SC
Blake A, Kineke G, Milligan T, Alexander C (2001) Sediment trapping and transport in the ACE Basin, South Carolina. Estuaries 24:721–733
Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205
Collins MR, Smith TI, Post WC, Pashuk O (2000) Habitat utilization and biological characteristics of adult Atlantic sturgeon in two South Carolina rivers. Trans Am Fish Soc 129:982–988
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Darden T, Tarpey C (2014) Genetic characterization of the Savannah and Pee Dee River populations of robust redhorse (Moxostoma robustum) with conservation implications. Copeia 2014:70–78
Dunton KJ, Chapman D, Jordaan A, Feldheim K, O’Leary SJ, McKown 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
Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361
Erickson DL, Kahnle A, Millard MJ, Mora EA, Bryja M, Higgs A, Mohler J, DuFour M, Kenney G, Sweka J, Pikitch EK (2011) Use of pop-up satellite archival tags to identify oceanic-migratory patterns for adult Atlantic sturgeon, Acipenser oxyrinchus oxyrinchus Mitchell, 1815. J Appl Ichthyol 27:356–365
Estoup A, Angers B (1998) Theoretical and empirical considerations. Adv. Mol Ecol 306:55
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
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
Henderson A, Spidle A, King T (2005) Genetic diversity, kinship analysis, and broodstock management of captive Atlantic sturgeon for population restoration. American Fisheries Society Symposium 2005:621–633
Henderson-Arzapalo A, King T (2002) Novel microsatellite markers for Atlantic sturgeon (Acipenser oxyrinchus) population delineation and broodstock management. Mol Ecol Notes 2:437–439
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 65–70
Jones OR, Wang J (2010) Colony: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
King T, Lubinski B, Spidle A (2001) Microsatellite DNA variation in Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) and cross-species amplification in the Acipenseridae. Conserv Genet 2:103–119
Kuo CH, Janzen FJ (2003) Bottlesim: a bottleneck simulation program for long-lived species with overlapping generations. Mol Ecol Notes 3:669–673
May B, Krueger CC, Kincaid HL (1997) Genetic variation at microsatellite loci in sturgeon: primer sequence homology in Acipenser and Scaphirhynchus. Can J Fish Aquat Sci 54:1542–1547
McCord JW, Collins MR, Post WC, Smith TI (2007) Attempts to develop an index of abundance for age-1 Atlantic sturgeon in South Carolina, USA. In: American Fisheries Society Symposium, p. 397. American Fisheries Society.
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution Int J org Evolution 60:2399–2402
Meirmans PG, Hedrick PW (2011) Assessing population structure: \({{F}_{ST}}\) and related measures. Mol Ecol Resour 11:5–18
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
Murawski SA, Pacheco AL (1977) Biological and fisheries data on Atlantic sturgeon, Acipenser oxyrhynchus (Mitchill). Sandy Hook Laboratory, Northeast Fisheries Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, US Department of Commerce.
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution, 354–362
Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461
NMFS (2012a) Endangered and threatened wildlife and plants; threatened and endangered status for distinct population segments of Atlantic sturgeon in the Northheast Region. Fed Reg 77:5880–5912
NMFS (2012b) Endangered and threatened wildlife and plants; final listing determinations for two distinct population segments of Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) in the Southeast. Fed Reg 77:5914–5982
O’Leary SJ, Dunton KJ, King TL, Frisk MG, Chapman DD (2014) 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
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539
Peterson DL, Bain MB, Haley N (2000) Evidence of declining recruitment of Atlantic sturgeon in the Hudson River. N Am J Fish Manage 20:231–238
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. J Hered 90:502–503
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rice WR (1989) Analyzing tables of statistical tests. Evolution, 223–225
Rodríguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Resour 12:873–884
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
Schueller P, Peterson DL (2010) Abundance and recruitment of juvenile Atlantic sturgeon in the Altamaha River, Georgia. Trans Am Fish Soc 139:1526–1535
Smith TI (1985) The fishery, biology, and management of Atlantic sturgeon, Acipenser oxyrhynchus, in North America. Environ Biol Fish 14:61–72
Smith TI, DE Marchette, GF Ulrich (1984) The Atlantic sturgeon fishery in South Carolina. N Am J Fish Manage 4:164–176
Smith JA, Flowers HJ, Hightower JE (2015) Fall spawning of Atlantic sturgeon in the Roanoke River, North Carolina. Trans Am Fish Soc 144:48–54
Tranah G, Campton DE, May B (2004) Genetic evidence for hybridization of pallid and shovelnose sturgeon. J Hered 95:474–480
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Waldman JR, Hart JT, Wirgin II (1996) Stock composition of the New York Bight Atlantic sturgeon fishery based on analysis of mitochondrial DNA. Trans Am Fish Soc 125:364–371
Waldman J, Grunwald C, Stabile J, Wirgin I (2002) Impacts of life history and biogeography on the genetic stock structure of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus, Gulf sturgeon A. oxyrinchus desotoi, and shortnose sturgeon A. brevirostrum. J Appl Ichthyol 18:509–518
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184
Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 1358–1370
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
Wirgin I, Waldman J, Stabile J, Lubinski B, King T (2002) Comparison of mitochondrial DNA control region sequence and microsatellite DNA analyses in estimating population structure and gene flow rates in Atlantic sturgeon Acipenser oxyrinchus. J Appl Ichthyol 18:313–319
Wirgin I, Maceda L, Waldman JR, Wehrell S, Dadswell M, King T (2012) Stock origin of migratory Atlantic sturgeon in Minas Basin, Inner Bay of Fundy, Canada, determined by microsatellite and mitochondrial DNA analyses. Trans Am Fish Soc 141:1389–1398
Acknowledgements
We would like to thank the assistance of J. Carter and National Oceanic and Atmospheric Administration (NOAA) Northwest Fisheries Science Center (NWFSC) Forensics Laboratory (formerly in Charleston, SC) for the archiving and access to Atlantic sturgeon genetic samples. We would also like to thank the Diadromous Fishes Research team at SCDNR for the collection of the samples, the Hollings Marine Laboratory for laboratory space, and the Fish Population Genetics research group at SCDNR for lab assistance, especially T. O’Donnell for laboratory optimization. This project was funded by a Sect. 6 Species Recovery Grants to States from the National Marine Fisheries Service (Grant No. NA13NMF4720044). This manuscript represents publication number 755 from the SCDNR Marine Resources Research Institute.
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Farrae, D.J., Post, W.C. & Darden, T.L. Genetic characterization of Atlantic sturgeon, Acipenser oxyrinchus oxyrinchus, in the Edisto River, South Carolina and identification of genetically discrete fall and spring spawning. Conserv Genet 18, 813–823 (2017). https://doi.org/10.1007/s10592-017-0929-7
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DOI: https://doi.org/10.1007/s10592-017-0929-7