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Genetic structure in lagoons: the effects of habitat discontinuity and low dispersal ability on populations of Atherina boyeri

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Abstract

Atherina boyeri is a common inhabitant of the Mediterranean brackish and coastal waters. Several recent studies proposed the recognition of three distinct forms/species (one lagoon/freshwater and two marine) within an A. boyeri complex. In this study, we used 10 newly available microsatellite loci to better define the genetic structure of the lagoon form. A total of 428 fishes from 11 lagoons along the Italian and Albanian coasts and three Italian lakes were analyzed. A pronounced genetic spatial structure was confirmed for all considered geographic scales (near, medium and broad). A restricted gene flow was detected, suggesting reduced population connectivity. The comparison of present data and previous studies, based on mtDNA and RAPD markers, allowed a preliminary identification of the roles of recent factors (gene flow, habitat discontinuity and water currents) and past events (e.g., Pleistocene glaciations) in shaping the pattern of genetic differentiation.

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References

  • Aldenhoven JT, Miller MA, Corneli PS, Shapiro MD (2010) Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits. Mol Ecol 19:4061–4076. doi:10.1111/j.1365-294X.2010.04801.x

    Article  CAS  Google Scholar 

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693. doi:10.1093/nar/25.22.4692

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Migliaccio M, Diaz-Almela E, Teixeira S, Van De Vliet MS, Alberto F, Procaccini G, Duarte CM, Serrão 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. doi:10.1111/j.1365-2699.2006.01671.x

    Article  Google Scholar 

  • Artegiani A, Bregant D, Paschini E, Pinardi F, Raicich F, Russo A (1997) The Adriatic Sea general circulation. Part II: baroclinic circulation structure. J Phys Oceanogr 27:1515–1532. doi:10.1175/1520-0485(1997)027<1515:TASGCP>2.0.CO;2

    Article  Google Scholar 

  • Astolfi L, Dupanloup I, Rossi R, Bisol PM, Faure E, Congiu L (2005) Mitochondrial variability of sand smelt Atherina boyeri populations from north Mediterranean coastal lagoons. Mar Ecol-Prog Ser 297:233–243. doi:10.3354/meps297233

    Article  CAS  Google Scholar 

  • Astraldi M, Balopoulos S, Candela J, Font J, Gacic M, Gasparini GP, Manca B, Theocharis A, Tintore J (1999) The role of straits and channels in understanding the characteristics of Mediterranean circulation. Prog Oceanogr 44:65–108. doi:10.1016/S0079-6611(99)00021-X

    Article  Google Scholar 

  • Bahri-Sfar L, Lemaire C, Ben Hassine OK, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc Roy Soc Lond B Bio 267:929–935. doi:10.1098/rspb.2000.1092

    Article  CAS  Google Scholar 

  • 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. doi:10.1073/pnas.081068098

    Article  CAS  Google Scholar 

  • Beheregaray LB, Sunnucks P (2001) Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Mol Ecol 10:2849–2866. doi:10.1046/j.1365-294X.2001.t01-1-01406.x

    Article  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) Genetix 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire génome, populations, interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier

    Google Scholar 

  • Bisol PM, Gallini A, Prevedello S, Rianna E, Bernardinelli E, Franco A, Zane L (2007) Low variation at allozyme loci and differences between age classes at microsatellites in grass goby (Zosterisessor ophiocephalus) populations. Hydrobiologia 577:151–159. doi:10.1007/s10750-006-0424-5

    Article  CAS  Google Scholar 

  • Buonaccorsi VP, McDowell JR, Graves JE (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 10:1179–1196. doi:10.1046/j.1365-294X.2001.01270.x

    Article  CAS  Google Scholar 

  • Burridge CP, Versace VL (2007) Population genetic structuring in Acanthopagrus butcheri (Pisces: Sparidae): does low gene flow among estuaries apply to both sexes? Mar Biotechnol 9:33–44. doi:10.1007/s10126-006-6023-7

    Article  CAS  Google Scholar 

  • Carvalho GR (1993) Evolutionary aspects of fish distribution: genetic variability and adaptation. J Fish Biol 43:53–73. doi:10.1111/j.1095-8649.1993.tb01179.x

    Article  Google Scholar 

  • Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) Concordance between dispersal and mitochondrial gene flow: isolation by distance in a tropical teleost, Lates calcarifer (Australian barramundi). Heredity 80:187–197. doi:10.1038/sj.hdy.6882920

    Article  Google Scholar 

  • Congiu L, Rossi R, Colombo G (2002) Population analysis of the sand smelt Atherina boyeri (Teleostei Atherinidae), from Italian coastal lagoons by random amplified polymorphic DNA. Mar Ecol-Prog Ser 229:279–289. doi:10.3354/meps229279

    Article  CAS  Google Scholar 

  • Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  Google Scholar 

  • De Innocentiis S, Lesti A, Livi S, Rossi AR, Crosetti D, Sola L (2004) Microsatellite markers reveal population structure in gilthead sea bream Sparus auratus from the Atlantic Ocean and Mediterranean Sea. Fisheries Sci 70:852–859. doi:10.1111/j.1444-2906.2004.00879.x

    Article  Google Scholar 

  • DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473. doi:10.1006/jfbi.1999.1210

    Article  CAS  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x

    Article  CAS  Google Scholar 

  • Duvernell DD, Lindmeier JB, Faust KE, Whitehead A (2008) Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus. Mol Ecol 17:1344–1360. doi:10.1111/j.1365-294X.2007.03648.x

    Article  Google Scholar 

  • Eichwald CE (1838) Faunae Caspii maris primitiae. Bull Mosc Soc Nat 11:125–174

    Google Scholar 

  • Eschmeyer WN, Fricke R (2011) Catalog of fishes electronic version (14 July 2011). http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp

  • 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. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • Francisco SM, Cabral H, Vieira MN, Almada V (2006) Contrasts in genetic structure and historical demography of marine and riverine populations of Atherina at similar geographical scales. Estuar Coast Shelf Sci 69:655–661. doi:10.1016/j.ecss.2006.05.017

    Article  Google Scholar 

  • Francisco SM, Congiu L, Stefanni S, Castilho R, Brito A, Ivanova PP, Levy A, Cabral H, Kilias G, Doadrio I, Almada VC (2008) Phylogenetic relationships of the North-eastern Atlantic and Mediterranean forms of Atherina (Pisces, Atherinidae). Mol Phylogenet Evol 48:782–788. doi:10.1016/j.ympev.2007.12.009

    Article  CAS  Google Scholar 

  • Francisco SM, Congiu L, von der Heyden S, Almada VC (2011) Multilocus phylogenetic analysis of the genus Atherina (Pisces: Atherinidae). Mol Phylogenet Evol 61:71–78. doi:10.1016/j.ympev.2011.06.002

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Gysels ES, Hellemans B, Pampoulie C, Volckaert FAM (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Mol Ecol 13:403–417. doi:10.1046/j.1365-294X.2003.02087.x

    Article  CAS  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer, Sunderland

    Google Scholar 

  • Hauser L, Ward RD (1998) Population identification in pelagic fish: the limits of molecular markers. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, Amsterdam

    Google Scholar 

  • Huelsenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175:1787–1802. doi:10.1534/genetics.106.061317

    Article  CAS  Google Scholar 

  • Kiener A, Spillmann CJ (1969) Contributions à l’étude systématique et écologique des athérines des côtes françaises. Mém Mus Natl Hist Nat Sér A Zool 60:1–74

    Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    CAS  Google Scholar 

  • Klossa-Kilia E, Papasotiropoulos V, Tryfonopoulos G, Alahiotis S, Kilias G (2007) Phylogenetic relationships of Atherina hepsetus and Atherina boyeri (Pisces: Atherinidae) populations from Greece, based on mtDNA sequences. B J Linn Soc 92:151–161. doi:10.1111/j.1095-8312.2007.00829.x

    Article  Google Scholar 

  • Kottelat M (1997) European freshwater fishes. Biologia 52:1–271

    Google Scholar 

  • Lougheed SC, Gibbs HL, Prior KA, Weatherhead PJ (2000) A comparison of RAPD versus microsatellite DNA markers in population studies of the massasauga rattlesnake. J Hered 91:458–463. doi:10.1093/jhered/91.6.458

    Article  CAS  Google Scholar 

  • Maggio T, Lo Brutto S, Garoia F, Tinti F, Arculeo M (2009) Microsatellite analysis of red mullet Mullus barbatus (Perciformes, Mullidae) reveals the isolation of the Adriatic Basin in the Mediterranean Sea. ICES J Mar Sci 66:1883–1891. doi:10.1093/icesjms/fsp160

    Article  Google Scholar 

  • Maltagliati F (1999) Genetic divergence in natural populations of the Mediterranean brackish-water killifish Aphanius fasciatus. Mar Ecol-Prog Ser 179:155–162. doi:10.3354/meps179155

    Article  Google Scholar 

  • Milana V, Sola L, Congiu L, Rossi AR (2008) Mitochondrial DNA in Atherina (Teleostei, Atheriniformes): differential distribution of an intergenic spacer in lagoon and marine forms of Atherina boyeri. J Fish Biol 73:1216–1227. doi:10.1111/j.1095-8649.2008.01994.x

    Article  CAS  Google Scholar 

  • Milana V, Sola L, Rossi AR, Barbisan F, Congiu L (2009) Isolation, characterization and cross-species testing of microsatellites obtained from a sand smelt (Atherina boyeri) genomic library. Mol Ecol Resour 9:889–892. doi:10.1111/j.1755-0998.2008.02366.x

    Article  CAS  Google Scholar 

  • Miller-Sims VC, Gerlach G, Kingsford MJ, Atema J (2008) Dispersal in the spiny damselfish, Acanthochromis polyacanthus, a coral reef fish species without a larval pelagic stage. Mol Ecol 17:5036–5048. doi:10.1111/j.1365-294X.2008.03986.x

    Article  CAS  Google Scholar 

  • Mistri M, Colombo G (1988) Morphometric variability in sandsmalt, Atherina boyeri Risso 1810, populations from different Italian sites. B Zool 55:129–132. doi:10.1080/11250008809386608

    Article  Google Scholar 

  • Moretti G, Gianotti FS, Giganti A (1959) Il latterino (Atherina mochon Cuv.) nel Trasimeno (Biometria, regime dietetico, pesca e parassitismo). Riv Biol 51:3–38

    Google Scholar 

  • Moritz C (1994) Defining ‘Evolutionary Significant Units’ for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4

    Article  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  Google Scholar 

  • Nikula R, Vainola R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143:339–350. doi:10.1007/s00227-003-1088-6

    Article  Google Scholar 

  • O’Reilly PT, Canino MF, Bailey KM, Bentzen P (2004) Inverse relationship between F ST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure. Mol Ecol 13:1799–1814. doi:10.1111/j.1365-294X.2004.02214.x

    Article  Google Scholar 

  • Orr MR, Smith TB (1998) Ecology and speciation. Trends Ecol Evol 13:502–506. doi:10.1016/S0169-5347(98)01511-0

    Article  CAS  Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16. doi:10.1016/j.tree.2006.09.003

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. doi:10.1146/annurev.ecolsys.25.1.547

    Article  Google Scholar 

  • Peijnenburg KTCA, Fauvelot C, Breeuwer AJ, Menken SBJ (2006) Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers. Mol Ecol 15:3319–3338. doi:10.1111/j.1365-294X.2006.03002.x

    Article  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. doi:10.1093/jhered/esh074

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Quignard JP, Pras A (1986) Atherinidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-Eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 1207–1210

    Google Scholar 

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

    Google Scholar 

  • Rohling EJ, Bryden HL (1994) Estimating past changes in the Eastern Mediterranean fresh-water budget, using reconstructions of sea-level and hydrography. P K Ned Akad Wetensc 97:201–217

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  Google Scholar 

  • Sala B (2005) Mammalian faunas and environment from the Würmian Glacial Maximum of the Italian peninsula (approx. 22 ± ka cal BP). In: Fugagnoli A, Bassi D (eds) Giornata di Studi Paleontologici “Prof. C. Loriga Broglio”. Ann Univ Ferrara, Italy

    Google Scholar 

  • Sala-Bozano M, Ketmaier V, Mariani S (2009) Contrasting signals from multiple markers illuminate population connectivity in a marine fish. Mol Ecol 18:4811–4826. doi:10.1111/j.1365-294X.2009.04404.x

    Article  CAS  Google Scholar 

  • Stefanni S, Thorley JL (2003) Mitochondrial DNA phylogeography reveals the existence of an evolutionarily significant unit of the sand goby Pomatoschistus minutus in the Adriatic (Eastern Mediterranean). Mol Phylogenet Evol 28:601–609. doi:10.1016/S1055-7903(03)00054-X

    Article  CAS  Google Scholar 

  • Thiede L (1978) A glacial Mediterranean. Nature 276:680–683. doi:10.1038/276680a0

    Article  Google Scholar 

  • Trabelsi M, Faure E, Quignard JP, Boussaid M, Focante B, Mâamouri F (2002a) Atherina punctata and Atherina lagunae (Pisces, Atherinidae), new species in the Mediterranean Sea. 1. Biometric investigations of three Atherinid species. C R Biol 325:967–975. doi:S1631-0691(02)01506-8

    Article  Google Scholar 

  • Trabelsi M, Gilles A, Fleury C, Mâamouri F, Quignard JP, Faure E (2002b) Atherina punctata and Atherina lagunae (Pisces, Atherinidae), new species in the Mediterranean Sea. 2. Molecular investigations of three Atherinid species. C R Biol 325:1119–1128. doi:S1631-0691(02)01529-9

    Article  CAS  Google Scholar 

  • Trabelsi M, Mâamouri F, Quignard JP, Boussaid M, Faure E (2004) Morphometric or morpho-anatomal and genetic investigations highlight allopatric speciation in Western Mediterranean lagoons within the Atherina lagunae species (Teleostei, Atherinidae). Estuar Coast Shelf Sci 61:713–723. doi:10.1016/j.ecss.2004.07.011

    Article  CAS  Google Scholar 

  • 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 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400. doi:10.2307/2409146

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi:10.2307/2408641

    Article  Google Scholar 

  • Whittaker JC, Harbord RM, Boxall N, Mackay I, Dawson G, Sibly RM (2003) Likelihood-based estimation of microsatellite mutation rates. Genetics 164:781–787

    Google Scholar 

  • Williams DA, Brown SD, Crawford DL (2008) Contemporary and historical influences on the genetic structure of the estuarine-dependent Gulf killifish Fundulus grandis. Mar Ecol-Prog Ser 373:111–121. doi:10.3354/meps07742

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  Google Scholar 

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Acknowledgments

Financial support was provided by the University of Rome ‘La Sapienza’, Progetti di Ateneo 2007–2009. We thank all people who helped in the collection of sand smelts: D Crosetti (Institute for Environmental Protection and Research), Territorial Executive Office for Biodiversity of Fogliano, L Tancioni (University of Rome “Tor Vergata”), A Santulli (University of Palermo), IAM Marino (University of Padova), A Fusari and M Rampacci (Agriculture and Fish Management). We wish to thank the two anonymous reviewers who helped to improve this manuscript.

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  1. Department of Biology and Biotechnology, Sapienza University of Rome, 00161, Rome, Italy

    Valentina Milana, Luciana Sola, Elisa Angiulli & Anna Rita Rossi

  2. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457, Constance, Germany

    Paolo Franchini

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  1. Valentina Milana
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Correspondence to Luciana Sola.

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Communicated by T. Reusch.

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227_2011_1817_MOESM2_ESM.tif

Summary of sampling locations considered in the present and previous studies on lagoon and lake samples of A. boyeri. Circles and triangles indicate studies based on mitochondrial and nuclear markers, respectively. The color indicates the corresponding reference. See Table 1 in supplementary data for details on the type of the used molecular marker (TIFF 55814 kb)

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Milana, V., Franchini, P., Sola, L. et al. Genetic structure in lagoons: the effects of habitat discontinuity and low dispersal ability on populations of Atherina boyeri . Mar Biol 159, 399–411 (2012). https://doi.org/10.1007/s00227-011-1817-1

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