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.
Similar content being viewed by others
References
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 34:963–976
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 297:233–243
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 36:523–535
Baus E, Darrock DJ, Bruford MW (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Mol Ecol 14:3373–3382
Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035
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 98:4563–4568
Bianchi NC, Morri C (2000) Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar Poll Bullet 40:367–376
Blake RW (1976) On seahorse locomotion. J Mar Biol Assoc UK 56:939–949
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 40:1839–1849
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:e0116219
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, France
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 96:67–75
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 21:3671–3685
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 30:261–272
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
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 38:742–754
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
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 24:2713–2719
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 11:401
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 291:81–91
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 68:707–733
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 17:468–484
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 17:3873–3888
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 290:89–96
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 16:3592–3605
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 474:243–261
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
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, Lisher HEL (2010) Arlequin ver. 3.5: a new series of programs to perform population genetics analysis under Linux and Windows. Mol Ecol Resour 10:564–567
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 12:194
Foster SJ, Vincent ACJ (2004) Life history and ecology of seahorses: implications for conservation and management. J Fish Biol 65:1–61
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
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 106:1473–1478
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 7:638–640
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 19:3692–3707
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Universite de Lausanne, Lausanne
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 89:415–426
Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, Berkeley
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 83:561–576
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
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 11:1165–1176
Hudson RR, Slatkin M, Maddison WP (1992) Estimation of gene flow from DNA sequence data. Genetics 132:583–589
Jensen JL, Bohonah AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13
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 14:3219–3234
Kenchington E, Heino M, Nielsen EE (2003) Managing marine genetic diversity: time for action? ICES J Mar Sci 60:1172–1176
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:e0117538
Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ (2004) A guide to the identification of seahorses, Washington D.C.
Luzzatto DC, Estalles ML, Diaz de Astarloa JM (2013) Rafting seahorses: the presence of the seahorse Hippocampus patagonicus in floating debris. J Fish Biol 83:677–681
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–S122
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 39:734–746
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 53:596–601
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 58:395–403
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 12:78
Nicastro KR, Zardi GI, McQuaid CD, Teske PR, Barker NP (2008) Coastal topography drives genetic structure in marine mussels. Mar Ecol Prog Ser 368:189–195
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 485:123–142
Palsboll PJ, Berube M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16
Palumbi SR (2003) Population genetics, demographic connectivity and the design of marine reserves. Ecol Appl 13:S146–S158
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 8:1243–1245
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:e7268
Patarnello T, Volckaert FA, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444
Perante NC, Pajaro MG, Meeuwig JJ, Vincent ACJ (2002) Biology of a seahorse species, Hippocampus comes in the central Philippines. J Fish Biol 60:821–837
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 89:417–424
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 16:187–192
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 357:175–184
Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697
Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959
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 7:1041–1051
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 153:47–60
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 107:2102–2107
Rousset F (2008) GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Notes 8:103–106
Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol 6:600–602
Saarman NP, Louie KD, Hamilton H (2010) Genetic differentiation across eastern Pacific oceanographic barriers in the threatened seahorse Hippocampus ingens. Conserv Genet 11:1989–2000
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 82:856–876
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 20:5167–5181
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 19:557–568
Sorokin YI (2002) The Black Sea: ecology and oceanography. Backhuis Publishing, Leiden
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland
Teske PR, Cherry MI, Matthee CA (2003) Population genetics of the endangered Knysna seahorse, Hippocampus capensis. Mol Ecol 12:1703–1715
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 7:138
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 25:4876–4882
Vandendriessche S, Messiaen M, Vincx M, Degraer S (2005) Juvenile Hippocampus guttulatus from a neuston tow at the French-Belgian border. Belg J Zool 135:101–102
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 336:1383–1385
Vincent AC, Foster SJ, Koldewey HJ (2011) Conservation and management of seahorses and other Syngnathidae. J Fish Biol 78:1681–1724
Volkmann L, Martyn I, Moulton V, Spillner A, Mooers AO (2014) Prioritizing populations for conservation using phylogenetic networks. PLoS One 9:e88945
Ward RD, Woodmark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232
Wilson AB (2006) Genetic signature of recent glaciation on populations of a near-shore marine fish species (Syngnathus leptorhynchus). Mol Ecol 15:1857–1871
Wilson AB, Eigenmann Veraguth I (2010) The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol Ecol 19:4535–4553
Winnepenninckx B, Backeljau T, Dewachter R (1993) Extraction of high molecular-weight DNA from molluscs. Trends Genet 9:407
Woodall LC (2009) The population genetics and mating systems of European seahorses. PhD thesis, Royal Holloway-University of London, UK
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
Woodall LC, Koldewey HJ, Shaw PW (2011a) Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus. Conserv Genet 12:1645–1649
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 78:1738–1756
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 92:1427–1432
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:e42201
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Woodall, L.C., Koldewey, H.J., Boehm, J.T. et al. Past and present drivers of population structure in a small coastal fish, the European long snouted seahorse Hippocampus guttulatus . Conserv Genet 16, 1139–1153 (2015). https://doi.org/10.1007/s10592-015-0728-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-015-0728-y