Advertisement

Conservation Genetics

, Volume 16, Issue 5, pp 1139–1153 | Cite as

Past and present drivers of population structure in a small coastal fish, the European long snouted seahorse Hippocampus guttulatus

  • L. C. Woodall
  • H. J. Koldewey
  • J. T. Boehm
  • P. W. Shaw
Research Article

Abstract

The effective design of species conservation programs is reliant on information such as extant geographic distribution, taxon-specific life-history characteristics, and the relative influence of historic processes and contemporary environmental parameters in shaping population genetic diversity. Seahorses are weak swimmers and have a brooded young, limiting their dispersal potential. They live in sheltered locations, which are physically isolated from each other. Therefore panmixia across their geographic range is unlikely. Hippocampus guttulatus, a seahorse inhabiting European waters, has a geographic range spanning a number of contemporary oceanographic features that are proposed barriers to gene flow. Thus this fish is well-placed to test the contributions of environment and life-history factors in shaping population structuring. This study found that mitochondrial DNA and nuclear DNA (microsatellite) genotype data are concordant in suggesting that, like many other small fishes in European waters, H. guttulatus extant populations expanded from at least one southern European refugial population. Subsequent population differentiation of four geographic lineages reflects contemporary oceanographic barriers to gene flow. Demographic analyses suggest a northward, and long-term isolation between Black Sea and Mediterranean Sea populations. Moreover H. guttulatus contemporary population distribution and population structure are predominately explained by historic and oceanographic influences. These findings suggest that conservation of genetic diversity in H. guttulatus may be aided by a network of marine protected areas (MPAs), implemented to conserve coastal habitats, but the species’ unusual life history and gamete retaining behaviours should be considered as part of management decisions including MPA design and fisheries management plans.

Keywords

Hippocampus guttulatus Conservation genetics Phylogeography Europe Seahorse 

Notes

Acknowledgments

This is a contribution from Project Seahorse. We gratefully acknowledge France: C. L. Milinaire, P. Moriniere, S. Auffret, X. De Montandouin, P. Louisy, J-B Senegas, P. LeLong, Spain: J.A. Rodriguez, Scubadoo, A.Martinez de Murguia, B. Moya, Greece: F. Vilanikis, Y. Issaris, M. Salomidi, Tethys dive club, Thalassa, Portugal, Parque Natural da Ria Formosa, M. Gaspar, F. Gil, Italy: A. Tavaglini, S. Repetto, L. Castellano, Bulgaria: A. Seaman, T. Gallati, Gallati Divecenter, Volunteers: J. Marcus, V. Santos, D. Mason, M. Naud, T-T. Ang and S. DeAmicis for support with field work and providing samples. We also express thanks to J. Curtis and N. McKeown for enlightening discussion and technical assistance. Finally we wish to thank reviewers for their useful comments.

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

This project was funded by Chocolaterie Guylian and a Natural Environment Research Council Industrial Case studentship (NER/S/C/2005/13461) to LCW.

Supplementary material

10592_2015_728_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 12 kb)
10592_2015_728_MOESM2_ESM.docx (12 kb)
Supplementary material 2 (DOCX 12 kb)

References

  1. Arnaud-Haond S, Migliaccio M, Diaz-Almela E, Teixira S, Van de Vilet MS, Alberto F, Procaccini G, Duarte CM, Serrao EA (2007) Vicariance patterns in the Mediterranean Sea: east-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J Biogeogr 34:963–976CrossRefGoogle Scholar
  2. Astolfi L, Dupanloup I, Rossi R, Bisol PM, Faure E, Congiu L (2005) Mitochondrial variability of sand smelt Atherina boyeri populations from north Mediterranean costal lagoons. Mar Ecol Prog Ser 297:233–243CrossRefGoogle Scholar
  3. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Palma J, Patarnello T (2005) The Atlantic-Mediterranean transition: discordant genetic patterns in two seabream species Diplodus puntazzo (Cetti) and Diplodus sargus (L.). Mol Phylogenet Evol 36:523–535CrossRefPubMedGoogle Scholar
  4. Baus E, Darrock DJ, Bruford MW (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Mol Ecol 14:3373–3382CrossRefPubMedGoogle Scholar
  5. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035PubMedCentralPubMedGoogle Scholar
  6. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568CrossRefPubMedCentralPubMedGoogle Scholar
  7. Bianchi NC, Morri C (2000) Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar Poll Bullet 40:367–376CrossRefGoogle Scholar
  8. Blake RW (1976) On seahorse locomotion. J Mar Biol Assoc UK 56:939–949CrossRefGoogle Scholar
  9. Boehm JT, Woodall LC, Teske PR, Lourie SA, Baldwin C, Waldman J, Hickerman M (2013) Marine dispersal and barriers drive Atlantic seahorse diversification. J Biogeogr 40:1839–1849Google Scholar
  10. Boehm JT, Waldman J, Robinson JD, Hickerson MJ (2015) Population genomics reveals seahorses Hippocampus erectus of the western mid-Atlantic coast to be residents rather than vagrants. PLoS One 10:e0116219CrossRefPubMedCentralPubMedGoogle Scholar
  11. Boisseau J (1967) Les régulations hormonales de l’incubation chez un vertèbre male: recherches sur la reproduction de l’hippocampe. PhD thesis, L’Université de Bordeaux, FranceGoogle Scholar
  12. Caldwell IR, Vincent ACJ (2013) A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use. Environ Biol Fish 96:67–75CrossRefGoogle Scholar
  13. Casado-Amezua P, Goffredo S, Templado J, Machordom A (2012) Genetic assessment of population structure and connectivity in the threatened Mediterranean coral Astroides calycularis (Scleractinia, Dendrophylliidae) at different spatial scales. Mol Ecol 21:3671–3685CrossRefPubMedGoogle Scholar
  14. Casey SP, Hall HJ, Stanley HF, Vincent ACJ (2004) The origin and evolution of seahorses (genus Hippocampus): a phylogenetic study using the cytochrome b gene of mitochondrial DNA. Mol Phylogenet Evol 30:261–272CrossRefPubMedGoogle Scholar
  15. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  16. Charrier G, Chenel T, Durand JD, Girand M, Quiniou L, Laroche J (2006) Discrepancies in phylogeographical patterns of two European anglerfishes (Lophius budegassa and Lophius piscatorius). Mol Phylogenet Evol 38:742–754CrossRefPubMedGoogle Scholar
  17. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  18. Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a userfriendly approach to approximate Bayesian computation. Bioinfomatics 24:2713–2719CrossRefGoogle Scholar
  19. Cornuet J-M, Ravigne V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinform 11:401CrossRefGoogle Scholar
  20. Curtis JMR, Vincent ACJ (2005) Distribution of sympatric seahorse species along a gradient of habitat complexity in a seagrass-dominated community. Mar Ecol Prog Ser 291:81–91CrossRefGoogle Scholar
  21. Curtis JMR, Vincent ACJ (2006) Life history of an unusual marine fish: survival, growth and movement patterns of Hippocampus guttulatus Cuvier 1829. J Fish Biol 68:707–733CrossRefGoogle Scholar
  22. Curtis JMR, Ribeiro J, Erzini K, Vincent ACJ (2007) A conservation trade-off? Interspecific differences in seahorse responses to experimental changes in fishing effort. Aquat Conserv 17:468–484CrossRefGoogle Scholar
  23. Debes PV, Zachos FE, Hanel R (2008) Mitochondrial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic. Mol Ecol 17:3873–3888CrossRefPubMedGoogle Scholar
  24. Diekmann OE, Coyer JA, Ferreira J, Olsen JL, Stam WT, Pearson GA, Serrao EA (2005) Population genetics of Zostera noltii along the west Iberian coast: consequences of small population size, habitat discontinuity and near-shore currents. Mar Ecol Prog Ser 290:89–96CrossRefGoogle Scholar
  25. Domingues VS, Faria C, Stefanni S, Santos RS, Brito A, Almada VC (2007) Genetic divergence in the Atlantic-Mediterranean Montagu’s blenny, Coryphoblennius galerita (Linnaeus 1758) revealed by molecular and morphological characters. Mol Ecol 16:3592–3605CrossRefPubMedGoogle Scholar
  26. Durand JD, Blel H, Shen KN, Koutrakis ET, Guinand B (2013) Population genetic structure of Mugil cephalus in the Mediterranean and Black Seas: a single mitochondrial clade and many nuclear barriers. Mar Ecol Prog Ser 474:243–261CrossRefGoogle Scholar
  27. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  28. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  29. Excoffier L, Lisher HEL (2010) Arlequin ver. 3.5: a new series of programs to perform population genetics analysis under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  30. Faria R, Weiss S, Alexandrino P (2012) Comparative phylogeography and demographic history of European shads (Alosa alosa and A. fallax) inferred from mitochondrial DNA. BMC Evol Biol 12:194CrossRefPubMedCentralPubMedGoogle Scholar
  31. Foster SJ, Vincent ACJ (2004) Life history and ecology of seahorses: implications for conservation and management. J Fish Biol 65:1–61CrossRefGoogle Scholar
  32. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  33. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106:1473–1478CrossRefPubMedCentralPubMedGoogle Scholar
  34. Galbusera PHA, Gillemot S, Jouk P, Teske PR, Hellemans B, Volckaert AMJ (2007) Isolation of microsatellite markers for the endangered Knysna seahorse Hippocampus capensis and their use in the detection of a genetic bottleneck. Mol Ecol Notes 7:638–640CrossRefGoogle Scholar
  35. Galindo HM, Pfeiffer-Herbert AS, McManus MA, Chao Y, Chai F, Palumbi SR (2010) Seascape genetics along a steep cline: using genetic patterns to test predictions of marine larval dispersal. Mol Ecol 19:3692–3707CrossRefPubMedGoogle Scholar
  36. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Universite de Lausanne, LausanneGoogle Scholar
  37. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  38. Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, BerkeleyGoogle Scholar
  39. Gysels ES, Hellemans B, Patarnello T, Volckaerst FAM (2004) Current and historical gene flow of the sand goby Pomatoschistus minutus on the European Continental Shelf and in the Mediterranean Sea. Biol J Linn Soc 83:561–576CrossRefGoogle Scholar
  40. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  41. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  42. Hoarau G, Rijnsdorp AD, Van der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellite revealed large-scale spatial and temporary homogeneity. Mol Ecol 11:1165–1176CrossRefPubMedGoogle Scholar
  43. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of gene flow from DNA sequence data. Genetics 132:583–589PubMedCentralPubMedGoogle Scholar
  44. Jensen JL, Bohonah AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13CrossRefPubMedCentralPubMedGoogle Scholar
  45. Jorgensen HBH, Hansen MM, Bekkevold D, Ruzzante DE, Loeschcke V (2005) Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea. Mol Ecol 14:3219–3234CrossRefPubMedGoogle Scholar
  46. Kenchington E, Heino M, Nielsen EE (2003) Managing marine genetic diversity: time for action? ICES J Mar Sci 60:1172–1176CrossRefGoogle Scholar
  47. Lopez A, Vera M, Planas M, Bouza C (2015) Conservation genetics of threatened Hippocampus guttulatus in vulnerable habitats in NW Spain: temporal and spatial stability of wild populations with flexible polygamous mating system in captivity. PLoS One 10:e0117538CrossRefPubMedCentralPubMedGoogle Scholar
  48. Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ (2004) A guide to the identification of seahorses, Washington D.C.Google Scholar
  49. Luzzatto DC, Estalles ML, Diaz de Astarloa JM (2013) Rafting seahorses: the presence of the seahorse Hippocampus patagonicus in floating debris. J Fish Biol 83:677–681CrossRefPubMedGoogle Scholar
  50. Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Vainola R, Viard F, Wares J (2008) Evaluating valuating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89:S108–S122CrossRefPubMedGoogle Scholar
  51. Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746CrossRefPubMedGoogle Scholar
  52. Merji R, Lo Butto S, Ben Hassine OK, Arculeo M (2009) A study on Pomatoschistus tortonesei Miller 1968 (Perciformes, Gobiidae) reveals the Siculo-Tunisian Strait (STS) as a breakpoint for gene flow in the Mediterranean basin. Mol Phylogenet Evol 53:596–601CrossRefGoogle Scholar
  53. Merjri R, Arculeo M, Ben Hassine OK, Brutto SL (2011) Genetic architecture of the marbled goby Pomatoschistus marmoratus (Perciformes, Gobiidae) in the Mediterranean Sea. Mol Phylogenet Evol 58:395–403CrossRefGoogle Scholar
  54. Neiva J, Pearson GA, Valero M, Serrao EA (2012) Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L. BMC Evol Biol 12:78CrossRefPubMedCentralPubMedGoogle Scholar
  55. Nicastro KR, Zardi GI, McQuaid CD, Teske PR, Barker NP (2008) Coastal topography drives genetic structure in marine mussels. Mar Ecol Prog Ser 368:189–195CrossRefGoogle Scholar
  56. Nolasco R, Dubert J, Dominges CP, Cordeiro Piers A, Queiroga H (2013) Model-derived connectivity patterns along the western Iberian Peninsula: asymmetrical larval flow and source-sink cell. Mar Ecol Prog Ser 485:123–142CrossRefGoogle Scholar
  57. Palsboll PJ, Berube M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16CrossRefPubMedGoogle Scholar
  58. Palumbi SR (2003) Population genetics, demographic connectivity and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  59. Pardo BG, López A, Martínez P, Bouza C (2006) Novel microsatellite loci in the threatened European long-snouted seahorse (Hippocampus guttulatus) for genetic diversity and parentage analysis. Conserv Genet 8:1243–1245CrossRefGoogle Scholar
  60. Pascoal S, Creer S, Taylor MI, Queiroga H, Carvalho G, Mendo S (2009) Development and application of microsatellites in Carcinus maenas: genetic differentiation between northern and central Portuguese populations. PLoS One 4:e7268CrossRefPubMedCentralPubMedGoogle Scholar
  61. Patarnello T, Volckaert FA, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444CrossRefPubMedGoogle Scholar
  62. Perante NC, Pajaro MG, Meeuwig JJ, Vincent ACJ (2002) Biology of a seahorse species, Hippocampus comes in the central Philippines. J Fish Biol 60:821–837CrossRefGoogle Scholar
  63. Perez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424CrossRefPubMedGoogle Scholar
  64. Pérez-Ruzafa A, Marcos C, García-Charton JA, Salas F (2008) European marine protected areas (MPAs) as tools for fisheries management and conservation. J Nat Conserv 16:187–192CrossRefGoogle Scholar
  65. Piñeira J, Quesada H, Rolán-Alvarez E, Caballero A (2008) Genetic discontinuity associated with an environmentally induced barrier to gene exchange in the marine snail Littorina saxatilis. Mar Ecol Prog Ser 357:175–184CrossRefGoogle Scholar
  66. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697CrossRefPubMedCentralPubMedGoogle Scholar
  67. Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  68. Quesada H, Gallagher C, Skibinski DAG, Skibinski DOF (1998) Patterns of polymorphism and gene flow of gender- associated mitochondrial DNA lineages in European mussel populations. Mol Ecol 7:1041–1051CrossRefGoogle Scholar
  69. Quinteiro J, Rodriguez-Castro J, Rey-Mendez M (2007) Population genetic structure of the stalked barnacle Pollicipes pollicipes (Gmelin, 1789) in the North Eastern Atlantic: influence of coastal currents and mesoscale hydrographic structures. Mar Biol 153:47–60CrossRefGoogle Scholar
  70. Riccioni G, Landi M, Ferrara G, Milano I, Cariani A, Zane L, Sella M, Barbujan G, Tinti F (2010) Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic Bluefin tuna of the Mediterranean Sea. Proc Natl Acad Sci USA 107:2102–2107CrossRefPubMedCentralPubMedGoogle Scholar
  71. Rousset F (2008) GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Notes 8:103–106CrossRefGoogle Scholar
  72. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol 6:600–602CrossRefGoogle Scholar
  73. Saarman NP, Louie KD, Hamilton H (2010) Genetic differentiation across eastern Pacific oceanographic barriers in the threatened seahorse Hippocampus ingens. Conserv Genet 11:1989–2000CrossRefGoogle Scholar
  74. Sanna D, Biagi F, Alaya HB, Maltagliati F, Addis A, Romero A, De Juan J, Quignard J-P, Castelli A, Franzoi P, Torricelli P, Casu M, Carcupino M, Francalacci P (2013) Mitochondrial DNA variability of the pipefish Syngnathus abaster. J Fish Biol 82:856–876CrossRefPubMedGoogle Scholar
  75. Schunter C, Carreras-Carbonell J, Macpherson E, Tintore J, Vidal-Vijande E, Pascual A, Guidetti P, Pascual M (2011) Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol Ecol 20:5167–5181CrossRefPubMedGoogle Scholar
  76. Serra IA, Innocenti AM, Dimaida G, Calvo S, Migliaccio M, Zambianchi E, Pizzigalli C, Arnaud-Haond S, Duarte CM, Serrao EA, Procaccini G (2010) Genetic structure in the Mediterranean seagrass Posidonia oceanica: disentangling past vicariance events from contemporary patterns of gene flow. Mol Ecol 19:557–568CrossRefPubMedGoogle Scholar
  77. Sorokin YI (2002) The Black Sea: ecology and oceanography. Backhuis Publishing, LeidenGoogle Scholar
  78. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, SunderlandGoogle Scholar
  79. Teske PR, Cherry MI, Matthee CA (2003) Population genetics of the endangered Knysna seahorse, Hippocampus capensis. Mol Ecol 12:1703–1715CrossRefPubMedGoogle Scholar
  80. Teske PR, Hamilton H, Matthee CA, Barker NP (2007) Signatures of seaway closures and founder dispersal in the phylogeny of a circumglobally distributed seahorse lineage. BMC Evol Biol 7:138CrossRefPubMedCentralPubMedGoogle Scholar
  81. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedCentralPubMedGoogle Scholar
  82. Vandendriessche S, Messiaen M, Vincx M, Degraer S (2005) Juvenile Hippocampus guttulatus from a neuston tow at the French-Belgian border. Belg J Zool 135:101–102Google Scholar
  83. Veitch L, Dulvy NK, Koldewey HJ, Lieberman S, Pauly D, Roberts CM, Rodgers AD, Baillie JEM (2012) Avoiding empty ocean commitments at Rio+ 20. Science 336:1383–1385CrossRefPubMedGoogle Scholar
  84. Vincent AC, Foster SJ, Koldewey HJ (2011) Conservation and management of seahorses and other Syngnathidae. J Fish Biol 78:1681–1724CrossRefPubMedGoogle Scholar
  85. Volkmann L, Martyn I, Moulton V, Spillner A, Mooers AO (2014) Prioritizing populations for conservation using phylogenetic networks. PLoS One 9:e88945CrossRefPubMedCentralPubMedGoogle Scholar
  86. Ward RD, Woodmark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232CrossRefGoogle Scholar
  87. Wilson AB (2006) Genetic signature of recent glaciation on populations of a near-shore marine fish species (Syngnathus leptorhynchus). Mol Ecol 15:1857–1871CrossRefPubMedGoogle Scholar
  88. Wilson AB, Eigenmann Veraguth I (2010) The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol Ecol 19:4535–4553CrossRefPubMedGoogle Scholar
  89. Winnepenninckx B, Backeljau T, Dewachter R (1993) Extraction of high molecular-weight DNA from molluscs. Trends Genet 9:407CrossRefPubMedGoogle Scholar
  90. Woodall LC (2009) The population genetics and mating systems of European seahorses. PhD thesis, Royal Holloway-University of London, UKGoogle Scholar
  91. Woodall LC (2012) Hippocampus guttulatus. In: IUCN 2013. IUCN Red List of Threatened Species, Version 2013.1 http://www.iucnredlist.org. Assessed 24 Nov 2013
  92. Woodall LC, Koldewey HJ, Shaw PW (2011a) Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus. Conserv Genet 12:1645–1649CrossRefGoogle Scholar
  93. Woodall LC, Koldewey HJ, Shaw PW (2011b) Historical and contemporary population genetic connectivity of the European short-snouted seahorse Hippocampus hippocampus and implications for management. J Fish Biol 78:1738–1756CrossRefPubMedGoogle Scholar
  94. Woodall LC, Jones R, Zimmerman B, Guillaume S, Stubbington T, Shaw P, Koldewey HJ (2012) Partial fin-clipping as an effective tool for tissue sampling seahorses, Hippocampus spp. J Mar Biol Assoc UK 92:1427–1432CrossRefGoogle Scholar
  95. Zarraonaindia I, Iriondo M, Albaina A, Pardo MP, Manzano C, Grant WS, Irigoien X, Estonba A (2012) Multiple SNP markers reveal fine-scale population and deep phylogeographic structure in European anchovy (Engraulis encrasicolus L.). PLoS One 7:e42201CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • L. C. Woodall
    • 1
    • 2
  • H. J. Koldewey
    • 3
  • J. T. Boehm
    • 4
  • P. W. Shaw
    • 1
    • 5
  1. 1.Royal HollowayUniversity of LondonSurreyUK
  2. 2.Natural History MuseumLondonUK
  3. 3.Zoological Society of LondonLondonUK
  4. 4.City College of New YorkNew YorkUSA
  5. 5.Aberystwyth UniversityCeredigionUK

Personalised recommendations