Skip to main content

Advertisement

Log in

Population genetic structure of protected allis shad (Alosa alosa) and twaite shad (Alosa fallax)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Determining the magnitude of homing behaviour within migratory fish species is essential for their conservation and management. We tested for population genetic structuring in the anadromous alosines, Alosa alosa and A. fallax fallax, to establish fidelity of stocks to spawning grounds in the United Kingdom and Ireland. Considerable genetic differences were present among populations of both species, suggesting strong fidelity to breeding grounds and compatible with homing to natal origins. Moreover, the genetic structure of A. fallax fallax showed a clear pattern of isolation-by-distance, consistent with breeding populations exchanging migrants primarily with neighbouring populations. Spatial genetic differences were on average much greater than temporal differences, indicating relatively stable genetic structure. Comparing anadromous A. fallax fallax populations to the landlocked Killarney shad subspecies, A. fallax killarnensis (Ireland), demonstrated a long history of separation. These results demonstrating regional stock structure within the British Isles will inform practical management of stocks and their spawning habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexandrino PJ, Ferrand N, Rocha J (1996) Genetic polymorphism of a haemoglobin chain and adenosine deaminase in European shads: evidence for the existence of two distinct genetic entities with natural hybridization. J Fish Biol 48:447–456

    Article  CAS  Google Scholar 

  • Alexandrino PJ, Faria R, Linhares D, Castro F, Le Corre M, Sabatié MR, Baglinière J-L, Weiss S (2006) Interspecific differentiation and intraspecific substructure in two closely related clupeids with extensive hybridization, Alosa alosa and Alosa fallax. J Fish Biol 69(Supp B):242–259

    Article  CAS  Google Scholar 

  • Aprahamian MW, Lester SM (2001) Variation in the age at first spawning of female twaite shad (Alosa fallax fallax) from the River Severn, England. Bull Français de la Pêche et de la Pisciculture 362(363):941–951

    Article  Google Scholar 

  • Aprahamian MW, Baglinière J-L, Sabatié MR, Alexandrino PJ, Thiel R, Aprahamian CD (2003a) Biology, status, and conservation of the anadromous Atlantic twaite shad Alosa fallax fallax. Am Fish Soc Symp 35:103–124

    Google Scholar 

  • Aprahamian MW, Aprahamian CD, Baglinière J-L, Sabatié MR, Alexandrino PJ (2003b). Alosa alosa and Alosa fallax spp.: literature review and bibliography. RandD technical report W1-014/TR. Environment Agency, Bristol

  • Baglinière J-L, Sabatié MR, Rochard E, Alexandrino PJ, Aprahamian MW (2003) The allis shad Alosa alosa: Biology, ecology, range, and status of populations. Am Fish Soc Symp 35:85–102

    Google Scholar 

  • Boisneau P, Menesson-Boisneau C, Guyomard R (1992) Electrophoretic identity between Allis shad, Alosa alosa (L.), and Twaite shad, Alosa fallax (Lacépède). J Fish Biol 40:731–738

    Article  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    CAS  Google Scholar 

  • Ciborowski KL, Consuegra S, Garcia de Leaniz C, Wang J, Beaumont M, Jordan WC (2007) Stocking may increase mitochondrial DNA diversity but fails to halt the decline of endangered Atlantic salmon populations. Cons Biol 8:1355–1367

    CAS  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multi-locus molecular markers. Mol Ecol 15:2833–2843

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Coscia I, Rountree V, King JJ, Roche WK, Mariani S (2010) A highly permeable species boundary between two anadromous fishes. J Fish Biol 77:1137–1149

    Article  CAS  Google Scholar 

  • Doherty D, Maoleidigh NO, McCarthy TK (2004) The biology, ecology and future conservation of Twaite shad (Alosa fallax Lacépède), Allis shad (Alosa alosa L.) and Killarney shad (Alosa fallax killarnensis Tate Regan) in Ireland. Biol Environ Proc R Ir Acad 104B:93–102

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S. (2005) Arlequin (version. 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

  • Faria R, Wallner B, Weiss S, Alexandrino PJ (2004) Isolation and characterization of eight dinucleotide microsatellite loci from two closely related clupeid species (Alosa alosa and A. fallax). Mol Ecol Notes 4:586–588

    Article  CAS  Google Scholar 

  • Faria R, Weiss S, Alexandrino PJ (2006) A molecular phylogenetic perspective on the evolutionary history of Alosa spp. (Clupeidae). Mol Phylogenet Evol 40:298–304

    Article  CAS  Google Scholar 

  • Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S, Aubin-Horth N, Lajus D, Letcher BH, Youngson AF, Webb JH, Vøllestad LA, Villanueva B, Ferguson A, Quinn TP (2007) A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev 82:173–211

    Article  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F- statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (1999) PCA-Gen version 1.2. Institute of Ecology, Biology Building, University of Lausanne (UNIL), Lausanne

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

  • Hasselman DJ (2008) Comments on ‘Weak population differentiation in northern European populations of the endangered anadromous clupeid Alosa fallax. J Fish Biol 73:1096–1098

    Article  Google Scholar 

  • 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 67:1021–1039

    Article  CAS  Google Scholar 

  • Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362

    Google Scholar 

  • Hendricks ML, Hoopes RL, Arnold DA, Kaufmann ML (2002) Homing of hatchery-reared American shad to the Lehigh River, a tributary to the Delaware River. N Am J Fish Manage 22:243–248

    Google Scholar 

  • Jolly MT, Maitland PS, Genner MJ (2011) Genetic monitoring of two decades of hybridisation between allis shad (Alosa alosa) and twaite shad (Alosa fallax). Conserv Genet 12(4):1087–1100

    Article  Google Scholar 

  • Julian SE, Barton ML (2007) Microsatellite DNA markers for American shad (Alosa sapidissima) and cross-species amplification within the family Clupeidae. Mol Ecol Notes 7:805–807

    Article  CAS  Google Scholar 

  • King JJ, Roche WK (2008) Aspects of anadromous Allis shad (Alosa alosa Linnaeus) and Twaite shad (Alosa fallax Lacepede) biology in four Irish Special Areas of Conservation (SACs): status spawning indications and implications for conservation designation. Hydrobiologia 602:145–154

    Article  Google Scholar 

  • Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographic scales at Major Histocompatibility Complex and microsatellite in a philopatric fish (Salmo salar). Mol Ecol 10:2525–2540

    Google Scholar 

  • Lassalle G, Trancart T, Lambert P, Rochard E (2008) Latitudinal variations in age and size at maturity among allis shad Alosa alosa populations. J Fish Biol 73:1799–1809

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DNASP v5: software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • Limburg KE, Waldman JR (2009) Dramatic declines in North Atlantic diadromous fishes. Bioscience 59:955–996

    Article  Google Scholar 

  • Maes J, Stevens M, Breine J (2008) Poor water quality constrains the distribution and movements of twaite shad Alosa fallax fallax (Lacepede, 1803) in the watershed of river Scheldt. Hydrobiologia 602:129–143

    Article  Google Scholar 

  • Maitland PS, Hatton-Ellis TW (2003) Ecology of the Allis and Twaite Shad. Conserving natura 2000 rivers ecology series no. 3. English Nature, Peterborough

  • Maitland PS, Lyle AA (2005) Ecology of allis shad Alosa alosa and twaite shad Alosa fallax in the Solway Firth, Scotland. Hydrobiologia 534:205–221

    Article  Google Scholar 

  • Melvin GD, Dadswell MJ, Martin JD (1986) Fidelity of American shad, Alosa sapidissima (Clupeidae), to its river of previous spawning. Can J Fish Aquat Sci 43:640–646

    Article  Google Scholar 

  • O’Maoleidigh N, Cawdrey S, Bracken JJ, Ferguson A (1988) Morphometric, meristic character and electrophoretic analyses of two Irish populations of twaite shad, Alosa fallax (Lacepede). J Fish Biol 32:355–366

    Article  Google Scholar 

  • 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 17:582–597

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Rakaj N, Crivelli AJ (2001) Occurrence of agone Alosa agone in Lake Shkodra, Albania in sympatry with twaite shad Alosa fallax nilotica. B Fr Peche Piscic 362(363):1067–1073

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP version 1.2: populations genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Regan CT (1912) The twaite shad in Killarney lakes. Ir Nat 21:63

    Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Thiel R, Riel P, Neumann R, Winkler HM, Bottcher U, Grohsler T (2008) Return of twaite shad Alosa fallax (Lacepede, 1803) to the Southern Baltic Sea and the transitional area between the Baltic and North Seas. Hydrobiologia 602:161–177

    Article  Google Scholar 

  • Thorrold SR, Campana SE, Jones CM, McLaren JW, Lam JWH (1998) Trace element signatures in otoliths accurately record natal river of juvenile American shad (Alosa sapidissima). Limnol Oceanog 43:1826–1835

    Google Scholar 

  • Trewavas E (1938) The Killarney Shad or Goureen (Alosa fallax killarnensis, Regan 1916). Proc Linn Soc Lond 150:110–112

    Article  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Volk J, Bekkevold D, Loeschcke V (2007) Weak population differentiation in northern European populations of the endangered anadromous clupeid Alosa fallax. J Fish Biol 71(Supp C):461–469

    Article  Google Scholar 

  • Waldman JR, Grunwald C, Wirgin I (2008) Sea lamprey Petromyzon marinus: an exception to the rule of homing in anadromous fishes. Biol Lett 6:659–662

    Article  Google Scholar 

  • Walther BD, Thorrold SR (2008) Continental-scale variation in otolith geochemistry of juvenile American shad (Alosa sapidissima). Can J Fish Aquat Sci 65:2623–2635

    Article  CAS  Google Scholar 

  • Waters JM, Epifanio JM, Gunter T, Brown BL (2000) Homing behaviour facilitates subtle genetic differentiation among river populations of Alosa sapidissima: microsatellites and mtDNA. J Fish Biol 56:622–636

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jane Coghill and Keith Edwards from the Transcriptomics Facility at the University of Bristol for help with genotyping. This work was funded by the Esmee Fairbairn Foundation. MJG was supported by a Great Western Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin J. Genner.

Additional information

Communicated by M. I. Taylor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 122 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jolly, M.T., Aprahamian, M.W., Hawkins, S.J. et al. Population genetic structure of protected allis shad (Alosa alosa) and twaite shad (Alosa fallax). Mar Biol 159, 675–687 (2012). https://doi.org/10.1007/s00227-011-1845-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1845-x

Keywords

Navigation