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Conservation Genetics

, Volume 15, Issue 6, pp 1281–1298 | Cite as

Genetic diversity and structure of two hybridizing anadromous fishes (Alosa pseudoharengus, Alosa aestivalis) across the northern portion of their ranges

  • Meghan C. McBrideEmail author
  • Theodore V. Willis
  • Rod G. Bradford
  • Paul Bentzen
Research Article

Abstract

Alewife (Alosa pseudoharengus) and blueback herring (Alosa aestivalis), also known collectively as either river herring or gaspereau, are anadromous clupeid fishes that display spatiotemporal overlap during riverine spawning migrations. Both species have experienced severe population declines within portions of their ranges. Evidence that they home to their natal rivers to spawn suggests the likelihood of ecologically significant population structure, yet this hypothesis has not been rigorously tested. We examined genetic diversity, differentiation and population structure in 34 alewife and four blueback herring populations spanning a 2,500 km portion of their northern range, using 14 microsatellite loci. Significant differentiation was detected among most rivers, and eight genetically defined alewife population clusters that largely corresponded to hydrographic regions were identified. Similar population structure was seen for blueback herring. Genetic isolation by distance was not significant among alewife populations in regions that have been historically influenced by dams, and/or stock transfers, but was highly significant in two regions that have not been subject to these influences. Genetic differentiation of alewife populations was strongest in the Bay of Fundy. Bottleneck tests revealed evidence of demographic bottlenecks in all of the alewife populations. Lastly, our results indicated that hybridization between alewife and blueback herring is common.

Keywords

Population structure Genetic differentiation River herring Gaspereau Hybridization Population bottlenecks 

Notes

Acknowledgments

This research was supported by a Natural Sciences and Engineering Research Council Discovery Grant to P. Bentzen and Department of Interior, US Fish and Wildlife Service Coastal Program Grant (No. 501818G257), Department of Commerce, National Marine Fisheries Service Grant, National Fish and Wildlife Foundation (No. NSN-60365), National Science Foundation Grant (No. EPS-0904155) to Maine EPSCoR at the University of Maine. We thank Unama’ki Institute of Natural Resources, Sackville River Association, Petitcodiac Watershed Alliance, Tusket Gaspereau Dip Netters Association, commercial gaspereau fishers, Parks Canada, Department of Fisheries and Ocean and Maine Department of Marine Resources for their cooperation and aid in obtaining samples. Additionally, we thank J. Rivard, C. Glibbery, D. Keith, P. Debes, G. McCracken and E. MacLeod for their assistance in the field and I. Paterson in the lab.

Supplementary material

10592_2014_617_MOESM1_ESM.docx (517 kb)
Supplementary material 1 (DOCX 517 kb)

References

  1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323CrossRefGoogle Scholar
  2. Atlantic State Marine Fisheries Commission (ASFMC) (2009) Amendment 2 to the interstate fishery management plan for Shad and River Herring (River Herring Management). ASFMC, Washington DCGoogle Scholar
  3. Atlantic States Marine Fisheries Commission (ASMFC) (1985) Fishery management plan for the anadromous alosid stocks of eastern United States: American shad, hickory shad, Alewife, and blueback herring: phase II in interstate management planning for migratory alosids of the Atlantic Coast. ASMFC, Washington DCGoogle Scholar
  4. Bams RA (1976) Survival and propensity for homing as affected by presence or absence of locally adapted paternal genes in two transplanted populations of pink salmon (Oncorhynchus gorbuscha). J Fish Res Board Can 33:2716–2725CrossRefGoogle Scholar
  5. Bentzen P, Paterson I (2005) Genetic analyses of freshwater and anadromous alewife (Alosa pseudoharengus) populations from the St. Croix River, Maine/New Brunswick. Final Report to Maine Rivers, 3 Wade Street, Augusta, MaineGoogle Scholar
  6. Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. Fishery Bulletin 74 of the Fishery Bulletin of the Fish and Wildlife Service, 53. United States Government Printing Office, Washington, D.CGoogle Scholar
  7. Bouzat JL, Johnson JA, Toepfer JE, Simpson SA, Esker TL, Westemeier RL (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201CrossRefGoogle Scholar
  8. Bradbury IR, Campana SE, Bentzen P (2008) Low genetic connectivity in an estuarine fish with pelagic larvae. Can J Fish Aquat Sci 65:147–158CrossRefGoogle Scholar
  9. Bradford RG, Bentzen P, Campbell DM, Cook AM, Gibson AJF, Whitelaw J (2010) 2009 Update Status Report for Atlantic Whitefish (Coregonus huntsmani). DFO Canadian Science Advisory Secretariat Research Document 2010/005, p 39Google Scholar
  10. Bradford RG, LeBlanc P, Bentzen P (2012) Update Status Report on Bay of Fundy Striped Bass (Morone saxatilis). DFO Canadian Science Advisory Secretariat 2012/021, p 46Google Scholar
  11. Committee on the Status of Endangered Wildlife Canada (COSEWIC) (2011) Guidelines for recognizing designatable units. COSEWIC, Ottawa. http://www.cosewic.gc.ca/eng/sct2/sct2_5_e.cfm. Accessed 20 Jan 2012
  12. Coscia I, Rountree V, King JJ, Roche WK, Mariani S (2010) A highly permeable species boundary between two anadromous fishes. J Fish Biol 77:1137–1149PubMedCrossRefGoogle Scholar
  13. Coulson M (2014) Historical and contemporary processes shaping population genetic struction in an anadromous fish (Osmerus mordax). Ph.D. Thesis. Dalhousie University, HalifaxGoogle Scholar
  14. Crane J (2009) “Setting the river free”: the removal of the Edwards dam and the restoration of the Kennebec River. Water Hist 1:131–148CrossRefGoogle Scholar
  15. Curry RA (2007) Late glacial impacts on dispersal and colonization of Atlantic Canada and Maine by freshwater fishes. Quatern Res 67:225–233CrossRefGoogle Scholar
  16. Dadswell MJ, Rulifson RA, Daborn GR (1986) Potential impact of large-scale tidal power developments in the upper bay of Fundy on fisheries resources of the Northwest Atlantic. Fisheries 11:26–35CrossRefGoogle Scholar
  17. Dadswell MJ, Melvin GD, Williams PJ, Themelis DE (1987) Influences of origin, life history, and chance on the Atlantic coast migration of American shad. Am Fish Soc Symp 1:313–330Google Scholar
  18. Dashtgard SE, Pearson NJ, Gingras MK (2013) Sedimentology, icnology, ecology and anthropogenic modification of muddy tidal flats in a cold-temperate environment: Chignecto Bay, Canada. Geological Society of London, London. doi: 10.1144/SP388.3 Google Scholar
  19. Davis JP, Schultz ET (2009) Temporal shifts in demography and life history of an anadromous alewife population in Connecticut. Mar Coast Fish Dyn Manag Ecosyst Sci 1:90–106CrossRefGoogle Scholar
  20. Department of Fisheries and Oceans (DFO) (2001) Gaspereau Maritime Provinces Overview. DFO Science Stock Status Report D3-17. p 15Google Scholar
  21. Department of Fisheries and Oceans (DFO) (2007) Assessment of Gaspereau River Alewife. DFO Canadian Science Advisory Secretariat Science Advisory Report 2007/003. p 8Google Scholar
  22. Department of Fisheries and Oceans (DFO) (2012) Integrated Gaspereau Fishery Management Plan Eastern New Brunswick Area Gulf Region. p 51Google Scholar
  23. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:1–3CrossRefGoogle Scholar
  24. Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320CrossRefGoogle Scholar
  25. Engle VD, Summers JK (1999) Latitudinal gradients in benthic community composition in Western Atlantic estuaries. J Biogeogr 26:1007–1023CrossRefGoogle Scholar
  26. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  27. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  28. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  29. Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fish 6:379–416CrossRefGoogle Scholar
  30. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  31. Hall CJ, Jordaan A, Frisk MG (2011) The historic influence of dams on diadromous fish habitat with a focus on river herring and hydrologic longitudinal connectivity. Landsc Ecol 26:95–107CrossRefGoogle Scholar
  32. Hall CJ, Jordaan A, Frisk MG (2012) Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. Bioscience 62:723–731CrossRefGoogle Scholar
  33. Hardie DC, Hutchings JA (2010) Evolutionary ecology at the extremes of species’ ranges. Environ Rev 18:1–20CrossRefGoogle Scholar
  34. Hasselman DJ, Limburg KE (2012) Alosine Restoration in the 21st Century: challenging the Status Quo. Mar Coast Fish 4:174–187CrossRefGoogle Scholar
  35. Hasselman DJ, Bradford RG, Bentzen P (2010) Taking stock: defining populations of American shad (Alosa sapidissima) in Canada using neutral genetic markers. Can J Fish Aquat Sci 67:1021–1039CrossRefGoogle Scholar
  36. Hasselman DJ, Ricard D, Bentzen P (2013) Genetic diversity and differentiation in a wide ranging anadromous fish, American shad (Alosa sapidissima), is correlated with latitude. Mol Ecol 22:1558–1573PubMedCrossRefGoogle Scholar
  37. Hasselman DJ, Argo EE, McBride MC, Bentzen P, Schultz TF, Perez-Umphrey AA, Palkovacs EP (2014) Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Mol Ecol 23:1137–1152PubMedCrossRefGoogle Scholar
  38. Havey KA (1961) Restoration of anadromous alewives at Long Pond, Maine. Trans Am Fish Soc 90:281–286CrossRefGoogle Scholar
  39. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedCrossRefGoogle Scholar
  40. Hilborn R, Quinn TP, Schindler DE, Rogers DE (2003) Biocomplexity and fisheries sustainability. Proc Natl Acad Sci 100:6564–6568PubMedCentralPubMedCrossRefGoogle Scholar
  41. Hildebrand SF, Schroeder WC (1928) Fishes of Chesapeake Bay. Fishery Bulletin 43 of the United States Fish and Wildlife Service 1:1–366Google Scholar
  42. Hutchinson WF (2008) The dangers of ignoring stock complexity in fishery management: the case of the North Sea cod. Biol Lett 4:693–695PubMedCentralPubMedCrossRefGoogle Scholar
  43. Hutchinson DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914CrossRefGoogle Scholar
  44. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  45. Jessop B, Anderson W (1989) Effects of heterogeneity in the spatial and temporal pattern of juvenile alewife (Alosa pseudoharengus) and blueback herring (A. aestivalis) density on estimation of an index of abundance. Can J Fish Aquat Sci 46:1564–1574CrossRefGoogle Scholar
  46. Jolly MT, Maitland PS, Genner MJ (2011) Genetic monitoring of two decades of hybridization between allis shad (Alosa alosa) and twaite shad (Alosa fallax). Conserv Genet 12:1087–1100CrossRefGoogle Scholar
  47. Julian SE, Bartron ML (2007) Microsatellite DNA markers for American shad (Alosa sapidissima) and cross-species amplification within the family Clupeidae. Mol Ecol Notes 7:805–807CrossRefGoogle Scholar
  48. Labbe EM (2012) Influence of stocking history and geography on the population genetics of alewife (Alosa pseudoharengus) in Maine rivers. M.Sc. Thesis, University of Southern MaineGoogle Scholar
  49. Labbe EM, Argo EE, Schultz TF, Palkovacs EP, Willis TV (2012) Multiplex microsatellite markers for river herring (Alosa pseudoharengus, Alosa aestivalis). Molecular Ecology Resources Primer Development Consortium. Permanent genetic resources note. Mol Ecol Res 12:185–189CrossRefGoogle Scholar
  50. Langella O (1999) Populations 1.2.30: a population genetic software. CNRS UPR9034. http://bioinformatics.org/~tryphon/populations
  51. Leberg P (2008) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449CrossRefGoogle Scholar
  52. Leim AH, Scott WB (1966) Fishes of the Atlantic coast of Canada. Bulletin No 155. Fisheries Research Board of Canada, Ottawa, p 485Google Scholar
  53. Limburg KE, Hattala KA, Kahnle A (2003) American shad in its native range. In: Limburg KE, Waldman JR (eds). Biodiversity, status, and conservation of the world’s shads. American Fisheries Society Symposium 35, Maryland, pp 125–140Google Scholar
  54. Loesch JG (1987) Overview of life history aspects of anadromous Alewife and blueback herring in freshwater habitats. In: Dadswell MJ, Klauda RJ, Moffitt CM, Sounders RL (eds). Common strategies of anadromous and catadromous fishes. American Fisheries Society Symposium 1, Maryland, pp 89–103Google Scholar
  55. Loesch JG, Kriete WH, Foell EJ (1982) Effects of light intensity on the catchability of juvenile anadromous Alosa species. Trans Am Fish Soc 111:41–44CrossRefGoogle Scholar
  56. Mach ME, Sbrocco EJ, Hice LA, Duffy TA, Conover DO, Barber PH (2011) Regional differentiation and post-glacial expansion of the Atlantic silverside, Menidia menidia, an annual fish with high dispersal potential. Mar Biol 158:515–530PubMedCentralPubMedCrossRefGoogle Scholar
  57. Maine Department of Environmental Protection (MDEP) (2009) January 1, 2009 status reports: hydropower projects in maine, DEPLW0363-2009, and Dam Removals in Maine and Dams Subject to Regulated Minimum Flow ReleasesGoogle Scholar
  58. Maitland PS, Lyle AA (2005) Ecology of Allis Shad Alosa alosa and Twaite Shad Alosa fallax in the Solway Firth, Scotland. Hydrobiologia 534:205–221CrossRefGoogle Scholar
  59. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190PubMedCrossRefGoogle Scholar
  60. McBride M (2013) Population Structure of River Herring (Alewife, Alosa pseudoharengus, and Blueback Herring, Alosa aestivalis) Examined using neutral genetic markers. M.Sc. Thesis, Dalhousie UniversityGoogle Scholar
  61. McConnell SKJ, Ruzzante DE, O’Reilly PT, Hamilton L, Wright JM (1997) Microsatellite loci reveal highly significant genetic differentiation among Atlantic salmon (Salmo salar L.) stocks fromt eh east coast of Canada. Mol Ecol 6:1075–1089CrossRefGoogle Scholar
  62. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402PubMedCrossRefGoogle Scholar
  63. Messieh SN (1977) Population structure and biology of alewives (Alosa pseudoharengus) and blueback herring (A. aestivalis) in the Saint John River, New Brunswick. Environ Biol Fish 2:195–210CrossRefGoogle Scholar
  64. Nei M (1972) Genetic distance between populations. Am Nat 106:283–392CrossRefGoogle Scholar
  65. Neves R (1981) Offshore distribution of alewife, Alosa pseudoharengus, and blueback herring, Alosa aestivalis, along the Atlantic coast. Fish Bull Seattle 79:473–485Google Scholar
  66. NOAA National Marine Fisheries Service (2009) Species of Concern: River herring (Alewife and Blueback herring) Alosa pseudoharengus and A. aestivalis. Silver Spring, MarylandGoogle Scholar
  67. NOAA National Marine Fisheries Service (2013) Endangered and threatened wildlife and plants; endangered species act listing determination for alewife and blueback herring. Fed Reg 79:48944–48994Google Scholar
  68. Page RDM (1996) TreeView. An application to display phylogenetic trees on personal computer. Comp Appl Biol Sci 12:357–358Google Scholar
  69. Palkovacs EP, Dion KB, Post DM, Caccone A (2008) Independent evolutionary origins of landlocked alewife populations and rapid parallel evolution of phenotypic traits. Mol Ecol 17:582–597PubMedCrossRefGoogle Scholar
  70. Palkovacs EP, Hasselman DJ, Argo EE, Gephard SR, Limburg KE, Post DM, Schultz TF, Willis TV (2013) Combining genetic and demographic information to prioritize conservation efforts for anadromous alewife and blueback herring. Evol Appl 7:212–226PubMedCentralPubMedCrossRefGoogle Scholar
  71. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  72. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency. J Hered 90:502–503CrossRefGoogle Scholar
  73. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  74. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  75. Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10:361–395CrossRefGoogle Scholar
  76. Reyer HU (2008) Mating with the wrong species can be right. Trends Ecol Evol 23:289–292PubMedCrossRefGoogle Scholar
  77. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  78. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  79. Rounsefell GA, Stringer LD (1945) Restoration and management of the New England alewife fisheries with special reference to Maine. US Department of the Interior, Fish and Wildlife Service. Trans Am Fish Soc 73:394–424CrossRefGoogle Scholar
  80. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedCentralPubMedGoogle Scholar
  81. Roy D, Hurlbut TR, Ruzzante DE, Fraser DJ (2012) Biocomplexity in a demersal exploited fish, white hake (Urophycis tenuis): depth-related structure and inadequacy of current management approaches. Can J Fish Aquat Sci 69:415–429CrossRefGoogle Scholar
  82. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  83. Scudder GGE (1989) The adaptive significance of marginal populations: a general perspective. Can Spec Publ Fish Aquat Sci 105:376–389Google Scholar
  84. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  85. Spidle AP, Kalinowski ST, Lubinski BA, Perkins DL, Blenad KF, Kocik JF, King TL (2003) Population structure of Atlantic Salmon in Maine with reference to populations from Atlantic Canada. Trans Am Fish Soc 132:196–209CrossRefGoogle Scholar
  86. Stabell OB (1984) Homing and olfaction in salmonids-a critical review with a special reference to the Atlantic salmon. Biol Rev Camb Philos Soc 59:333–388CrossRefGoogle Scholar
  87. Stone HH, Daborn GR (1987) Diet of alewives, Alosa pseudoharengus and blueback herring, A. aestivalis (Pisces: Clupeidae) in Minas Basin, Nova Scotia, a turbid, macrotidal estuary. Environ Biol Fish 19:55–67CrossRefGoogle Scholar
  88. Stone H, Jessop B (1992) Seasonal distribution of river herring Alosa pseudoharengus and A. aestivalis off the Atlantic coast of Nova Scotia. Fish Bull 90:376–389Google Scholar
  89. Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72PubMedCrossRefGoogle Scholar
  90. Vähä JP, Erkinaro J, Niemela E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654PubMedCrossRefGoogle Scholar
  91. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  92. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756CrossRefGoogle Scholar
  93. Waples RS, Do C (2009) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262PubMedCentralCrossRefGoogle Scholar
  94. Waters J, Epifanio J, Gunter T, Brown B (2000) Homing behaviour facilitates subtle genetic differentiation among river populations of Alosa sapidissima: microsatellites and mtDNA. J Fish Biol 56:622–636CrossRefGoogle Scholar
  95. Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  96. Williams RO, Grey WF, Huff JA (1975) Study anadromous fishes of Florida. Completion report for the period 1 May 1971 to 30 June 1974 for research funded by the Anadromous Fish Act (PL 89-304). National Marine Fisheries Service, St. Petersburg, FL, USA. http://research.myfwc.com/publications/search.asp. Accessed 16 Jan 2012

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Meghan C. McBride
    • 1
    Email author
  • Theodore V. Willis
    • 2
  • Rod G. Bradford
    • 3
  • Paul Bentzen
    • 1
  1. 1.Marine Gene Probe Laboratory, Biology DepartmentDalhousie UniversityHalifaxCanada
  2. 2.Environmental ScienceUniversity of Southern MaineGorhamUSA
  3. 3.Fisheries and Oceans CanadaBedford Institute of OceanographyDartmouthCanada

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