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The periwinkle Echinolittorina punctata (Mollusca: Gastropoda) tracked the warming of the Mediterranean Sea following the Last Glacial Maximum

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Abstract

Distribution shifts of intertidal species have been thoroughly described for several organisms on the Atlantic coasts of Europe, but comparatively less work has been conducted in the Mediterranean Sea. However, such semi-enclosed basins react faster to global change. The periwinkle Echinolittorina punctata is a littorinid gastropod which has shown a remarkable range expansion during the last few decades. Moreover, its unambiguous taxonomy, accessible habitat and ease of identification qualify it as an ideal descriptor of biotic changes in the Mediterranean Sea. We investigated genetic differentiation among 17 Mediterranean and Atlantic populations covering its current distributional range, using the mitochondrial cox1 marker to test the hypothesis that it experienced a significant range expansion triggered by sea warming after the Last Glacial Maximum (LGM). This would confirm its suitability as descriptor of climatic fluctuations. E. punctata has a weak population structure along its distributional range, with greater haplotype diversity in the western African populations than in the Mediterranean Sea, suggesting a recent population expansion following a bottleneck event. Such range expansion is dated ca. 15,000 years BP, and is, thus, related to the end of LGM. E. punctata planktotrophic development lasts 3–4 weeks, likely triggering the weak population structure and enhanced ability to track environmental change.

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References

  • Albano PG (2010) Further northward extension of the distribution of Echinolittorina punctata (Mollusca: Gastropoda) along the Italian Tyrrhenian coastline: new stations in Lazio. Cah Biol Mar 51:201–204

    Google Scholar 

  • Albano PG (2014) Recent changes in the distribution of autochthonous marine molluscs in the Mediterranean Sea. In: Goffredo S, Dubinsky Z (ed) The Mediterranean Sea: its history and present challenges, 1st edn, vol 17. Springer, Dordrecht, pp 307–318

    Chapter  Google Scholar 

  • Albano PG (2015) New records of Echinolittorina punctata (Gastropoda: Littorinidae) in the Mediterranean Sea from Italy, France and Greece. Mar Biodivers Rec 8:e3

    Article  Google Scholar 

  • Albano PG, Trono D (2008) On the occurrence of Echinolittorina punctata (Gmelin, 1791) (Gastropoda: Littorinidae) in Puglia, South-Eastern Italy. Boll Malacol 44:123–126.

    Google Scholar 

  • Albano PG, Sabelli B, Adani M, Pinardi N (2010) The thermophilous species Echinolittorina punctata as a new descriptor of tropicalization in the Mediterranean Sea-first data. Biol Mar Medit 17(1):90–93

    Google Scholar 

  • Almada F, Levy A, Robalo JI (2016) Not so sluggish: the success of the Felimare picta complex (Gastropoda, Nudibranchia) crossing Atlantic biogeographic barriers. PeerJ 4:e1561

    Article  Google Scholar 

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

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Ecol 16:37–48

    CAS  Google Scholar 

  • Birchenough SNR, Reiss H, Degraer S, Mieszkowska N, Borja Á, Buhl-Mortensen L, Braeckman U, Craeymeersch J, De Mesel I, Kerckhof F, Kröncke I, Parra S, Rabaut M, Schröder A, Van Colen C, Van Hoey G, Vincx M, Wätjen K (2015) Climate change and marine benthos: a review of existing research and future directions in the North Atlantic. WIREs Clim Chang 6:203–223

    Article  Google Scholar 

  • Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST2: a software platform for Bayesian evolutionary analysis. PLOS Comput Biol 10:e1003537

    Article  Google Scholar 

  • Bryden HL, Candela J, Kinder TH (1994) Exchange through the Strait of Gibraltar. Prog Oceanogr 33(3):201–248

    Article  Google Scholar 

  • Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES, Brander KM, Brown C, Bruno JF, Duarte CM, Halpern BS, Holding J, Kappel CV, Kiessling W, O’Connor MI, Pandolfi JM, Parmesan C, Schwing FB, Sydeman WJ, Richardson AJ (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–655

    Article  CAS  Google Scholar 

  • Cacho I, Grimalt JO, Canals M, Sbaffi L, Shackleton NJ, Schönfeld J, Zahn R (2001) Variability of the western Mediterranean Sea surface temperature during the last 25,000 years and its connection with the Northern Hemisphere climatic changes. Paleoceanography 16(1):40–52

    Article  Google Scholar 

  • Calderón I, Giribet G, Turon X (2008) Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Mar Biol 154:137–151

    Article  Google Scholar 

  • Dedah SO (1993) Wind, surface water temperature, surface salinity and pollution in the area of the Banc d’Arguin, Mauritania. Hydrobiol 258:9–19

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11(12):2571–2581

    Article  CAS  Google Scholar 

  • Duran S, Palacín C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328

    Article  CAS  Google Scholar 

  • Evangelisti F, Albano PG, Sabelli B (2010) Genetic variation of the brachiopod Gryphus vitreus (Born, 1778) across the Gibraltar sill. Biol Mar Medit 17(1):28–30

    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 10(3):564–567

    Article  Google Scholar 

  • Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359

    CAS  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  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol. Biotech 3:294–299

    CAS  Google Scholar 

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

    CAS  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 106(5):1473–1478

    Article  CAS  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 

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

    CAS  Google Scholar 

  • Helleberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848

    Article  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 Messinian salinity crisis. Nature 267:399–403

    Article  Google Scholar 

  • Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76:297–307

    Article  Google Scholar 

  • Ilves KL, Huang W, Wares JP, Hickerson MJ (2010) Colonization and⁄or mitochondrial selective sweeps across the North Atlantic intertidal assemblage revealed by multi-taxa approximate bayesian computation. Mol Ecol 19:4505–4519

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    Article  CAS  Google Scholar 

  • Launey S, Ledu C, Boudry P, Bonhomme F, Naciri-Graven Y (2002) Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by micro-satellite polymorphism. J Hered 93:331–338

    Article  CAS  Google Scholar 

  • Layton KKS, Martel AL, Hebert PDN (2014) Patterns of DNA barcode variation in Canadian marine molluscs. PLoS One 9(4):e95003. doi:10.1371/journal.pone.0095003

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5.10: a software for comprehensive analysis of DNA polymorphism data. Bioinform 25:1451–1451.

    Article  CAS  Google Scholar 

  • Lo Brutto S, Arculeo M, Parrinello N (2004) Congruence in genetic markers used to describe Mediterranean and Atlantic populations of European hake (Merluccius merluccius L. 1758). J Appl Ichthyol 20:81–86

    Article  Google Scholar 

  • Metz EC, Robles-Sikisaka R, Vacquier VD (1998) Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc Natl Acad Sci USA 95:10676–10681

    Article  CAS  Google Scholar 

  • Mieszkowska N (2009) Intertidal indicators of climate and global change. In: Letcher M (ed) Climate change: observed impacts on planet earth, 1st edn. Elsevier, Oxford, pp 281–296

    Chapter  Google Scholar 

  • Mieszkowska N, Kendall MA, Hawkins SJ, Leaper R, Williamson NJ, Hardman-Mountford NJ, Southward AJ (2006) Changes in the range of some common rocky shore species in Britain—a response to climate change? Hydrobiol 555:241–251

    Article  Google Scholar 

  • Mikolajewicz U (2011) Modeling Mediterranean Ocean climate of the Last Glacial Maximum. Clim Past 7:161–180

    Article  Google Scholar 

  • Milat T, Dragičević B, Nerlović V, Vrgoč S (2016) First record of Echinolittorina punctata (Gmelin, 1791) (Gastropoda) in the Adriatic Sea. Acta Adriat 57(1):179–182

    Google Scholar 

  • Palant B, Fishelson L (1968) Littorina punctata (Gmelin) and Littorina neritoides (L.), (Mollusca,Gastropoda) from Israel: ecology and annual cycle of genital system. Israel J Zool 17:145–160

    Google Scholar 

  • Palero F, Abelló P, Macpherson E, Cristina M, Pascual M (2008) Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Mol Phylogenet Evol 48:708–717

    Article  CAS  Google Scholar 

  • Palumbi SR (2003) Ecological subsidies alter the structure of marine communities. Proc Natl Acad Sci USA 100(21):11927–11928.

    Article  CAS  Google Scholar 

  • Patarnello T, Volckaert FMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16(21):4426–4444

    Article  Google Scholar 

  • Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925

    Article  Google Scholar 

  • Rambaut A, Drummond AJ, Suchard M (2014). Tracer v1.6. 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(12):2092–2100

    Article  CAS  Google Scholar 

  • Reid DG (2011) The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the eastern Atlantic Ocean and Mediterranean Sea. Zootaxa 2974:1–65

    Google Scholar 

  • Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006

    Article  Google Scholar 

  • Ríos C, Sanz S, Saavedra C, Peña JB (2002) Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P. maximus (L.) (Bivalvia: Pectinidae), across the Almeria–Oran Front. J Exp Mar Biol Ecol 267:223–244

    Article  Google Scholar 

  • Rogers AR (1995) Genetic evidence for a pleistocene population explosion. E 49(4):608–615

    Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9(3):552–569

    CAS  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

    Article  CAS  Google Scholar 

  • Rosewater J, Kadolsky D (1981) Rectifications in the nomenclature of some Indo-Pacific Littorinidae II. Proc Biol Soc Wash 94:1233–1236

    Google Scholar 

  • Rubal M, Veiga P, Cacabelos E, Moreira J, Sousa-Pinto I (2013) Increasing sea surface temperature and range shifts of intertidal gastropods along the Iberian Peninsula. J Sea Res 77:1–10

    Article  Google Scholar 

  • Sabelli B, Taviani M (2014) The making of the Mediterranean molluscan biodiversity. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: its history and present challenges. Springer, Dordrecht, pp 285–306

    Chapter  Google Scholar 

  • Sarà G, Milanese M, Prusina I, Sarà A, Angel DL, Glamuzina B, Nitzan T, Freeman S, Rinaldi A, Palmeri V, Montalto V, Lo Martire M, Gianguzza P, Arizza V, Lo Brutto S, De Pirro M, Helmuth B, Murray J, De Cantis S, Williams GA (2014) The impact of climate change on Mediterranean intertidal communities: losses in coastal ecosystem integrity and services. Reg Environ Chang 14(1):5–17

    Article  Google Scholar 

  • Sasson N, Simon-Blecher N, Achituv Y (2012) New molecular markers for revealing the population structure of Chthamalus stellatus in the Mediterranean and the eastern Atlantic. Mar Ecol Progr Ser 459:99–107

    Article  CAS  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Shackleton JC, van Andel TH, Runnels CN (1984) Coastal paleogeography of the central and western Mediterranean during the last 125,000 years and its archaeological implications. J Field Archaeol 11(3):307–314

    Google Scholar 

  • Shemesh E, Huchon D, Simon-Blecher N, Achituv Y (2009) The distribution and molecular diversity of the eastern Atlantic and Mediterranean chthamalids (Crustacea, Cirripedia). Zool Scr 38(4):365–378.

    Article  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  Google Scholar 

  • Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13:1377–1390

    Article  CAS  Google Scholar 

  • Struhsaker JW, Costlow JD (1968) Larval development of Littorina picta (Prosobranchia, Mesogastropoda), reared in the laboratory. Proc Malacol Soc Lond 38:153–160

    Google Scholar 

  • Sugiura N (1978) Further analysis of the data by akaike’s information criterion and the finite corrections. Commun Stat Theory. Methods 7:13–26

    Google Scholar 

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

    CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • 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(2):619–633

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tintore J, La Violette PE, Blade I, Cruzado A (1988) A study of an intense density front in the eastern Alboran Sea: the Almeria-Oran front. J Phys Oceanogr 18:1384–1397

    Article  Google Scholar 

  • Virgilio M, Fauvelot C, Costantini F, Abbiati M, Backeljau T (2009) Phylogeography of the common ragworm Hediste diversicolor (Polychaeta: Nereididae) reveals cryptic diversity and multiple colonization events across its distribution. Mol Ecol 18:1980–1994

    Article  CAS  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the north Atlantic intertidal. E 55(12):2455–2469

  • Williams ST, Reid DG (2004) Speciation and diversity on tropical rocky shores: a global phylogeny of snails of the genus Echinolittorina. E 58:2227–2251

    CAS  Google Scholar 

  • Wilson AB, Veraguth IE (2010) The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol Ecol 19:4535–4553

    Article  CAS  Google Scholar 

  • Winnepenninckx BT, Backeljau T, Deawachter R (1993) Complete small ribosomal subunit RNA sequence of the chiton Acanthopleura japonica (Lischke, 1873) (Mollusca, Polyplacophora). Nucleic Acids Res 21:1670

    Article  CAS  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  CAS  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  CAS  Google Scholar 

  • Zardoya R, Castilho R, Grande C, Favre-Krey L, Caetano S, Marcato S, Krey G, Patarnello T (2004) Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Mol Ecol 13:1785–1798

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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Acknowledgements

FE was funded by the Canziani Fund, Department of Biological, Geological and Environmental Sciences, University of Bologna. F. De Santis, B.S. Galil, S. Gofas, D. Grech, P. Ovalis, B. Öztürk, C. Palumbo, D.G. Reid and D. Trono sent samples from various localities in the Mediterranean Sea and West Africa. M. Passamonti commented on a first draft of the manuscript, M. Marzadori helped with figures, and F. Maltagliati and A. Luchetti provided suggestions on Bayesian analysis. D. Davoult, Executive Editor of Cahiers de Biologie Marine, authorized the reproduction of Fig. 1b, originally published in Albano (2010). Two anonymous reviewers provided useful suggestions to improve the manuscript.

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  1. Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Selmi 3, 40126, Bologna, Italy

    Francesca Evangelisti & Bruno Sabelli

  2. Department of Life and Environmental Sciences, Polytechnic University of Marche, Via Brecce Bianche, 60131, Ancona, Italy

    Alessandra Bellucci

  3. Department of Paleontology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Paolo G. Albano

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  1. Francesca Evangelisti
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  2. Alessandra Bellucci
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  4. Paolo G. Albano
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Evangelisti, F., Bellucci, A., Sabelli, B. et al. The periwinkle Echinolittorina punctata (Mollusca: Gastropoda) tracked the warming of the Mediterranean Sea following the Last Glacial Maximum. Mar Biol 164, 34 (2017). https://doi.org/10.1007/s00227-017-3071-7

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