Skip to main content

Advertisement

SpringerLink
Log in

Phylogeography of the littoral prawn species Palaemon elegans (Crustacea: Caridea: Palaemonidae) across the Mediterranean Sea unveils disparate patterns of population genetic structure and demographic history in the two sympatric genetic types II and III

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

Abstract

In this study, we examine the spatial distribution of genetic diversity of the littoral prawn species complex Palaemon elegans across the Mediterranean, with an emphasis in the eastern Mediterranean, and compare patterns of phylogeographic structure between the two genetic types II and III across potential gene flow barriers. For this purpose, a total of 293 mtDNA sequences of the cytochrome oxidase subunit-1 (Cox1) gene, including a newly generated dataset of 114 sequences, were obtained from 32 Mediterranean locations. The retrieved differences in genealogy and biogeographic patterns between both genetic types, as revealed by the outcome of a TCS statistical parsimony procedure, suggest different colonisation patterns in type II and type III within the Mediterranean. Furthermore, particular gradual transitions of both genetic types were unveiled across different geographic scales. Our results showed not only a marked latitudinal cline in the southeastern Mediterranean, but also a remarkable transition of the proportion of both types along the relatively small scale of the Italian coast. Detailed population genetic investigations and phylogeographic examinations within each genetic type datasets of P. elegans revealed evident and contrasting patterns of genetic structure in type II and type III. While the one-level analysis of molecular variance (AMOVA) resulted in significant genetic differentiation for both examined datasets, the outcome of multidimensional scaling (MDS), PERMUT, spatial analysis of molecular variance (SAMOVA) and two level-AMOVA analyses showed an obvious lack of phylogeographic structure within type II, versus significant population structuring within type III across known gene flow barriers in the Mediterranean. Notably, the outcome of isolation by distance (IBD) and isolation by environment (IBE) analyses within the type III dataset showed that both geographic and environmental distances were significant predictors of genetic distances. The remarkable difference in biogeographic patterns and demographic history [revealed mainly by Bayesian skyline plots (BSP) analysis] between both types suggests the likely involvement of different processes, including larval behaviour and/or residual effects of different phases of evolutionary history in the Mediterranean Sea.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Almaça C (1988) Competition, available space, and speciation in Mediterranean crabs. Ital J Zool 22(4):477–486

    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

    Google Scholar 

  • Arnaud-Haond S, Vonau V, Rouxel C, Bonhomme F, Prou J, Goyard E, Boudry P (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Mar Biol 155:147–157

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, pp 1–279

    Google Scholar 

  • Bahri-Sfar L, Lemaire C, Hassine OKB, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc R Soc B Biol Sci 267:929–935

    CAS  Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    CAS  PubMed  Google Scholar 

  • Béranger K, Mortier L, Gasparini GP, Gervasio L, Astraldi M, Crépon M (2004) The dynamics of the Sicily Strait: a comprehensive study from observations and models. Deep Sea Res II 51:411–440

    Google Scholar 

  • Berglund A (1980) Niche differentiation between two littoral prawns in Gullmar Fjord, Sweden: Palaemon adspersus and P. squilla. Ecography 3:111–115

    Google Scholar 

  • Berglund A, Bengtsson J (1981) Biotic and abiotic factors determining the distribution of two prawn species: Palaemon adspersus and P. squilla. Oecologia 49:300–304

    PubMed  Google Scholar 

  • Berglund A, Lagercrantz U (1983) Genetic differentiation in populations of two Palaemon prawn species at the Atlantic east coast: does gene flow prevent local adaptation? Mar Biol 77:49–57

    Google Scholar 

  • Bilgin R, Utkan MA, Kalkan E, Karhan SU, Bekbölet M (2015) DNA barcoding of twelve shrimp species (Crustacea: Decapoda) from Turkish seas reveals cryptic diversity. Medit Mar Sci 16(1):36–45

    Google Scholar 

  • Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186

    CAS  PubMed  Google Scholar 

  • Borrero-Pérez GH, González-Wangüemert M, Marcos C, Pérez-Ruzafa A (2011) Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Mol Ecol 20:1964–1975

    PubMed  Google Scholar 

  • Borsa P, Blanquer A, Berrebi P (1997) Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Mar Biol 129:233–246

    CAS  Google Scholar 

  • Calvo M, Templado J, Oliverio M, Machordom A (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biol J Linn Soc 96:898–912

    Google Scholar 

  • Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen J (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

    CAS  PubMed  Google Scholar 

  • Christie MR, Johnson DW, Stallings CD, Hixon MA (2010) Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Mol Ecol 19:1042–1057

    PubMed  Google Scholar 

  • Clement M, Posada DC, Crandall KA (2000) TCS: A computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    CAS  PubMed  Google Scholar 

  • Cognetti G, Maltagliati F (2000) Biodiversity and adaptive mechanisms in brackish water fauna. Mar Pollut Bull 40:7–14

    CAS  Google Scholar 

  • Costagliola D, Robertson DR, Guidetti P, Stefanni S, Wirtz P, Heiser JB, Bernardi G (2004) Evolution of coral reef fish Thalassoma spp. (Labridae). 2. Evolution of the eastern Atlantic species. Mar Biol 144:377–383

    Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    CAS  PubMed  Google Scholar 

  • Deli T, Chatti N, Said K, Schubart CD (2016a) Concordant patterns of mtDNA and nuclear phylogeographic structure reveal Pleistocene vicariant event in the green crab Carcinus aestuarii across the Siculo–Tunisian Strait. Mediterr Mar Sci 17(2):533–551

    Google Scholar 

  • Deli T, Fratini S, Ragionieri L, Said K, Chatti N, Schubart CD (2016b) Phylogeography of the marbled crab Pachygrapsus marmoratus (Decapoda, Grapsidae) along part of the African Mediterranean coast reveals genetic homogeneity across the Siculo–Tunisian Strait versus heterogeneity across the Gibraltar Strait. Mar Biol Res 12(5):471–487

    Google Scholar 

  • Derkarabetian S, Burns M, Starrett J, Hedin M (2016) Population genomic evidence for multiple Pliocene refugia in a montane-restricted harvestman (Arachnida, Opiliones, Sclerobunus robustus) from the southwestern United States. Mol Ecol 25:4611–4631

    PubMed  Google Scholar 

  • Domingues VS, Bucciarelli G, Almada VC, Bernardi G (2005) Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Mol Ecol 14:4051–4063

    PubMed  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro BE, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    CAS  PubMed  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    CAS  PubMed  Google Scholar 

  • Eckman JE (1996) Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. J Exp Mar Biol Ecol 200:207–237

    Google Scholar 

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864

    CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Fincham AA (1977) Larval development of British prawns and shrimps (Crustacea: Decapoda: Natantia): 1. Laboratory methods and a review of Palaemon (Paleander) elegans Rathke, 1837. Bull Br Mus Nat 31:1–28

    Google Scholar 

  • Fortunato C, Sbordoni V (1998) Allozyme variation in the Mediterranean rockpool prawn (Palaemon elegans): environmental vs. historical determinants. In: Proceedings and Abstracts of the Fourth International Crustacean Congress. Amsterdam, July 1998. Abstract: 12

  • Fratini S, Ragionieri L, Cutuli G, Vannini M, Cannicci S (2013) Pattern of genetic isolation in the crab Pachygrapsus marmoratus within the Tuscan archipelago (Mediterranean Sea). Mar Ecol Prog Ser 478:173–183

    Google Scholar 

  • Fratini S, Ragionieri L, Deli T, Harrer A, Marino IAM, Cannicci S, Zane L, Schubart CD (2016) Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference. BMC Evol Biol 16:150. doi:10.1186/s12862-016-0720-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 U S A 106:1473–1478

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grabowski M (2006) Rapid colonization of the polish Baltic coast by an Atlantic palaemonid shrimp Palaemon elegans Rathke, 1837. Aquat Invasions 1:116–123

    Google Scholar 

  • Grant WS (2015) Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. J Hered 106(4):333–346

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hamad N, Millot C, Taupier-Letage I (2006) The surface circulation in the eastern basin of the Mediterranean Sea. Sci Mar 70(3):457–503

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9

    Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66(4):591–600

    CAS  PubMed  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 

  • Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol Syst 40:291–310

    Google Scholar 

  • Hohenlohe PA (2004) Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around point conception, California. Biol J Linnean Soc 82:169–187

    Google Scholar 

  • Hsü KJ, Montadert L, Bernoulli D, Cita MB, Erickson A, Garrison RE, Kidd RB, Mèlierés F, Müller C, Wright R (1977) History of the Mediterranean salinity crisis. Nature 267:399–403

    Google Scholar 

  • Hudson RR (1990) Gene genealogies and the coalescent process. In: Futuyama D, Antonovics JD (eds) Oxford surveys in evolutionary biology. Oxford University Press, Oxford, pp 1–44

    Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    PubMed  PubMed Central  Google Scholar 

  • Johnson MS, Black R (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38:1371–1383

    PubMed  Google Scholar 

  • Jorde PE, Søvik G, Westgaard J-I, Albretsen J, André C, Hvingel C, Johansen T, Sandvik AD, Kingsley M, Jørstad KE (2015) Genetically distinct populations of northern shrimp, Pandalus borealis, in the North Atlantic: adaptation to different temperatures as an isolation factor. Mol Ecol 24:1742–1757

    PubMed  Google Scholar 

  • Kalkan E, Karhan SÜ, Yokes MB, Bilgin R (2013) The Turkish Straits System—phylogeographic break for the caridean shrimp Palaemon elegans (Crustacea: Decapoda). Rapp Comm Int Mer Médit 40:775

    Google Scholar 

  • Kordos LM, Burton RS (1993) Genetic differentiation of Texas Gulf Coast populations of the blue crab Callinectes sapidus. Mar Biol 117:227–233

    Google Scholar 

  • Kousteni V, Kasapidis P, Kotoulas G, Megalofonou P (2015) Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114:333–343. doi:10.1038/hdy.2014.107

    Article  CAS  PubMed  Google Scholar 

  • Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655

    CAS  Google Scholar 

  • Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206

    CAS  PubMed  Google Scholar 

  • Largier JL (1993) Estuarine fronts: how important are they? Estuar Coast 16:1–11

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lundquist CJ, Oldman JW, Lewis MJ (2009) Predicting suitability of cockle Austrovenus stutchburyi restoration sites using hydrodynamic models of larval dispersal. New Zeal J Mar Fresh Res 43:735–748

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Malanotte-Rizzoli P, Bergamasco A (1989) The circulation of the eastern Mediterranean. Part I. Oceanol Acta 12:335–351

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Manthey JD, Moyle RG (2015) Isolation by environment in White-breasted nuthatches (Sitta carolinensis) of the Madrean Archipelago sky islands: a landscape genomics approach. Mol Ecol 24:3628–3638

    CAS  PubMed  Google Scholar 

  • Marino IAM, Pujolar JM, Zane L (2011) Reconciling deep calibration and demographic history: Bayesian inference of post glacial colonization patterns in Carcinus aestuarii (Nardo, 1847) and C. maenas (Linnaeus, 1758). PLoS One 6(12):e28567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marko PB, Hart MW (2011) The complex analytical landscape of gene flow inference. Trends Ecol Evol 26:448–456

    PubMed  Google Scholar 

  • McMillen-Jackson AL, Bert TM (2004) Mitochondrial DNA variation and population genetic structure of the blue crab Callinectes sapidus in the eastern United States. Mar Biol 145:769–777

    CAS  Google Scholar 

  • Mejri R, Brutto SL, Hassine OKB, Arculeo M (2009) A study on Pomatoschistus tortonesei Miller 1968 (Perciformes, Gobiidae) reveals the Siculo–Tunisian Strait (STS) as a breakpoint to gene flow in the Mediterranean basin. Mol Phylogenet Evol 53:596–601

    CAS  PubMed  Google Scholar 

  • Millot C (2005) Circulation in the Mediterranean Sea: evidences, debates and unanswered questions. Sci Mar 69:5–21

    Google Scholar 

  • Millot C, Taupier-Letage I (2005) Circulation in the Mediterranean Sea. Hdb Env Chem 5:29–66

    CAS  Google Scholar 

  • Moraitou-Apostolopoulou M, Kiortsis V (1985) Mediterranean marine ecosystems. Plenum Press, New York, pp 1–407

    Google Scholar 

  • Muhs DR, Simmons KR, Steinke B (2002) Timing and warmth of the last interglacial period: new U-series evidence from Hawaii and Bermuda and a new fossil compilation for North America. J Quat Sci Rev 21:1355–1383

    Google Scholar 

  • Naro-Maciel E, Reid B, Holmes KE, Brumbaugh DR, Martin M, DeSalle R (2011) Mitochondrial DNA sequence variation in spiny lobsters: population expansion, panmixia, and divergence. Mar Biol 158:2027–2041

    CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nikula R, Väinölä R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143:339–350

    Google Scholar 

  • Nosil P, Funk DJ, Ortiz-Barrientos DA (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402

    PubMed  Google Scholar 

  • Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

    Google Scholar 

  • Pannacciulli FG, Bishop JDD, Hawkins SJ (1997) Genetic structure of populations of two species of Chthamalus (Crustacea: Cirripedia) in the north-east Atlantic and Mediterranean. Mar Biol 128:73–82

    Google Scholar 

  • Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444

    PubMed  Google Scholar 

  • Paula J (1998) Larval retention and dynamics of the prawns Palaemon longirostris H. Milne Edwards and Crangon crangon Linnaeus (Decapoda, Caridea) in the Mira estuary, Portugal. Invertebr Reprod Dev 33:221–228

    Google Scholar 

  • Peijnenburg KTCA, Fauvelot C, Breeuwer JA, Menken SB (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

    CAS  PubMed  Google Scholar 

  • Pelc RA, Warner RR, Gaines SD (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J Biogeogr 36:1881–1890

    Google Scholar 

  • Pérez-Losada MA, Nolte MJ, Crandall KA, Shaw PW (2007) Testing hypotheses of population structuring in the Northeast Atlantic Ocean and Mediterranean Sea using the common cuttlefish Sepia officinalis. Mol Ecol 16:2667–2679

    PubMed  Google Scholar 

  • Pérez-Portela R, Turon X (2008) Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 111:163–178

    PubMed  Google Scholar 

  • Petit RJ, Hampe A, Cheddadi R (2005) Climate changes and tree phylogeography in the Mediterranean. Taxon 54:877–885

    Google Scholar 

  • Pinardi N, Masetti E (2000) Variability of the large scale general circulation of the Mediterranean Sea from observations and modelling: a review. Paleogeogr Paleoclimatol Paleoecol 158:153–173

    Google Scholar 

  • Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56:378–399

    CAS  PubMed  Google Scholar 

  • Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity. Theor Appl Genet 90:462–470

    CAS  PubMed  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  PubMed  Google Scholar 

  • Quesada H, Beynon CM, Skibinski DOF (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: Pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524

    CAS  PubMed  Google Scholar 

  • Ragionieri L, Schubart CD (2013) Population genetics, gene flow, and biogeographical boundaries of Carcinus aestuarii (Crustacea: Brachyura: Carcinidae) along the European Mediterranean coast. Biol J Linnean Soc 109:771–790

    Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v 1.4.8. Institute of Evolutionary Biology, University of Edinburgh. Available from: http://beast.bio.ed.ac.uk/tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Reuschel S, Cuesta JA, Schubart CD (2010) Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Mol Phylogenet Evol 55:765–775

    PubMed  Google Scholar 

  • Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453

    CAS  PubMed  Google Scholar 

  • Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575

    Google Scholar 

  • Rolán-Alvarez E, Zapata C, Alvarez G (1995) Distinct genetic subdivision in sympatric and sibling species of the genus Littorina (Gastropoda: Littorinidae). Heredity 74:1–9

    PubMed  Google Scholar 

  • Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898

    CAS  PubMed  Google Scholar 

  • Roussenov V, Stanev E, Artale V, Pinardi N (1995) A seasonal model of the Mediterranean Sea general circulation. J Geophys Res 100:13515–13538

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schubart CD (2009) Mitochondrial DNA and decapod phylogenies: the importance of pseudogenes and primer optimization. In: Martin JW, Crandall KA, Felder DL (eds) Crustacean issues 18: decapod crustacean phylogenetics. Taylor & Francis/CRC Press, Boca Raton, Florida, pp 47–65

    Google Scholar 

  • Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365

    CAS  Google Scholar 

  • Schubart CD, Cuesta JA, Rodríguez A (2001) Molecular phylogeny of the crab genus Brachynotus (Brachyura: Varunidae) based on the 16S rRNA gene. Hydrobiologia 449:41–46

    Google Scholar 

  • Serena F (2005) Field identification guide to the sharks and rays of the Mediterranean and Black Sea. In: FAO species identification guide for fishery purposes. FAO, Rome, 97 pp

  • Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169

    Google Scholar 

  • Silberman JD, Sarver SK, Walsh PJ (1994) Mitochondrial DNA variation and population structure in the spiny lobster Panulirus argus. Mar Biol 120:601–608

    CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Singh SM, Green RH (1984) Excess of allozyme homozygosity in marine molluscs and its possible biological significance. Malacologia 25:569–581

    Google Scholar 

  • Svitoch AA, Selivanov AO, Yanina TA (2000) The Pont-Caspian and Mediterranean basins in the Pleistocene (paleogeography and correlation). Oceanology 40:868–881

    Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989) The effect of change in population size on DNA polymorphism. Genet Soc Amer 123:597–601

    CAS  Google Scholar 

  • Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285

    CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Technelysium Pty Ltd (2012) Chromas Lite ver. 2.1.1. Available from: http://www.technelysium.com.au/chromas_lite.html

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teske PR, Papadopoulos I, Zardi GI, McQuaid CD, Edkins MT, Griffiths CL, Barker NP (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152:697–711

    Google Scholar 

  • Thiede J (1978) A glacial Mediterranean. Nature 276:680–683

    Google Scholar 

  • Udekem d’Acoz C (1999) Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Collection “Patrimoines Naturels” (Muséum National d’Histoire Naturelle/S.P.N.), Paris

  • Wang IJ, Bradburd GS (2014) Isolation by environment. Mol Ecol 23:5649–5662

    PubMed  Google Scholar 

  • Wang IJ, Glor RE, Losos JB (2013) Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol Lett 16:175–182

    PubMed  Google Scholar 

  • Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44(2):213–232

    Google Scholar 

  • Watts RJ, Johnson MS (2004) Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Mar Freshw Res 55:641–651

    Google Scholar 

  • Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Google Scholar 

  • White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc Lond B 277:1685–1694

    Google Scholar 

  • Wilson MA, Curran HA, White B (1998) Paleontological evidence of a brief global sea-level event during the last interglacial. Lethaia 31(3):241–250

    Google Scholar 

  • Wing SR, Largier JL, Botsford LW, Quinn JF (1995) Settlement and transport of benthic invertebrates in an intermittent upwelling region. Limnol Oceanogr 40:316–329

    Google Scholar 

  • Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724

    CAS  PubMed  Google Scholar 

  • Zagwijn WH (1996) An analysis of Eemian climate in western and Central Europe. Quat Sci Rev 15:451–469

    Google Scholar 

  • Zenkevich LA (1963) Biology of the seas of the U.S.S.R. Interscience, New York

    Google Scholar 

  • Zitari-Chatti R, Chatti N, Fulgione D, Caiazza I, Aprea G, Elouaer A, Said K, Capriglione T (2009) Mitochondrial DNA variation in the caramote prawn Penaeus (melicertus) kerathurus across a transition zone in the Mediterranean Sea. Genetica 136:439–447

    CAS  PubMed  Google Scholar 

  • Zulliger DE, Tanner S, Ruch M, Ribi G (2009) Genetic structure of the high dispersal Atlanto-Mediterranean sea star Astropecten aranciacus revealed by mitochondrial DNA sequences and microsatellite loci. Mar Biol 156:597–610

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank those colleagues who facilitated material or accompanied during collections, among which are Silke Göttler (formally S. Reuschel) and José A. Cuesta for sequences from a previous study, Korbinian Eckel, Antje Elsäßer and Noah P. Schubart (North Cyprus), Nicolas Thiercelin (Paros), and Ayla A. and Sven O.P. Schubart (Alicante). Our special thanks are also extended to Hassan Hasan who provided us with samples from Latakia (Ibn Hani, Syria). In the laboratory and for statistical analyses, Korbinian Eckel and Nicolas Thiercelin rendered important support during the Bachelor thesis of Monika Pfaller. We thank Prof. Jürgen Heinze (University of Regensburg) for financial support of the laboratory work of the Bachelor students. We are also very grateful to Dr. Sammy De Grave and the two anonymous reviewers for their very helpful and interesting comments and suggestions to improve the quality of the manuscript.

Author information

Authors and Affiliations

  1. Laboratory of Genetics, Biodiversity and Enhancement of Bioresources (LR11ES41), University of Monastir, Higher Institute of Biotechnology of Monastir, Av. Tahar Hadded, B.P. 74, 5000, Monastir, Tunisia

    Temim Deli

  2. Zoology and Evolutionary Biology, University of Regensburg, 93040, Regensburg, Germany

    Monika Pfaller & Christoph D. Schubart

Authors
  1. Temim Deli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Pfaller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph D. Schubart
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Temim Deli.

Additional information

Communicated by S. De Grave

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deli, T., Pfaller, M. & Schubart, C.D. Phylogeography of the littoral prawn species Palaemon elegans (Crustacea: Caridea: Palaemonidae) across the Mediterranean Sea unveils disparate patterns of population genetic structure and demographic history in the two sympatric genetic types II and III. Mar Biodiv 48, 1979–2001 (2018). https://doi.org/10.1007/s12526-017-0711-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-017-0711-6

Keywords

Search

Navigation