Abstract
The present investigation focuses on population structure analysis of the purple sea urchin Paracentrotus lividus across the African Mediterranean coast, with the main aim of assessing the influence of the Siculo-Tunisian Strait on gene flow disruption in this highly dispersive echinoid species. For this purpose, patterns of morphological and genetic variation were assessed among its populations from the western and eastern Mediterranean coasts. A total of 302 specimens from seven Tunisian sites were collected and examined for morphometric variability at twelve morphometric traits. Concordant results, inferred from CDA (canonical discriminant analyses), pairwise NPMANOVA (non parametric multivariate analysis of variance) comparisons and MDS (multidimensional scaling) plot, unveiled significant inter-population differences in the measured traits among the studied populations. Furthermore, the combined use of the one way ANOSIM (analysis of similarities) and the Discriminant/Hotelling analysis allowed unravelling two morphologically differentiated groups assigned to both western and eastern Mediterranean basins. The SIMPER (similarity percentages) routine analysis showed that total dry weight, test diameter and spine length were major contributors to the morphometric separation between locations and between groups. Pattern of phenotypic divergence discerned in P. lividus across the Siculo-Tunisian Strait is interestingly in congruence with that inferred from the genetic investigation of the purple sea urchin populations from the same region based on the analysis of the mtDNA COI (cytochrome oxidase I) gene in 314 specimens from nineteen locations covering a wider geographic transect, streching westward to the Algerian coast and eastward to the Libyan littoral. The specific haplotypic composition characterizing each Mediterranean basin, as inferred from the minimum spanning network, confirmed the geographic partioning of genetic variation, as revealed by F-statistics and AMOVA (analysis of molecular variance) analyses, yielding significant genetic differentiation between eastern and western Mediterranean populations. The newly detected phylogeographic patterns, observed for the first time in P. lividus throughout the explored distribution range, suggest the involvement of different biotic and abiotic processes in shaping such variation, and provide evidence that a large and geographically exhaustive dataset is necessary to unveil phylogeographic structure within widespread marine species, previously cathegorized as panmictic in part of their distribution range.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Anastasiadou C, Leonardos I D. 2008. Morphological variation among populations of Atyaephyra desmarestii (Millet, 1831) (Decapoda: Caridea: Atyidae) from freshwater habitats of northwestern Greece. J Crustacean Biol, 28(2): 240–247
Anderson M J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol, 26(1): 32–46
Arculeo M, Brutto S L, Pancucci M P, et al. 1998. Allozyme similarity in two morphologically distinguishable populations of Paracentrotus lividus (Echinodermata) from distinct areas of the Mediterranean coast. J Mar Biol Assoc U K, 78: 231–238
Arnaud-Haond S, Migliaccio M, Diaz-Almela E, et al. 2007. Vicariance patterns in the Mediterranean Sea: east-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J Biogeogr, 34(6): 963–976
Bahri-Sfar L, Lemaire C, Hassine O K B, et al. 2000. Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc Roy Soc B: Biol Sci, 267(1446): 929–935
Barton N H, Hewitt G M. 1985. Analysis of hybrid zones. Ann Rev Ecol Syst, 16: 113–148
Béranger K, Mortier L, Gasparini G P, et al. 2004. The dynamics of the Sicily Strait: a comprehensive study from observations and models. Deep Sea Res II, 51(4-5): 411–440
Black R, Codd C, Hebbert D, et al. 1984. The functional significance of the relative size of Aristotle's lantern in the sea urchin Echinometramathaei (de Blainville). J Exp Mar Biol Ecol, 77(1-2): 81–97
Borsa P, Blanquer A, Berrebi P. 1997. Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Mar Biol, 129(2): 233–246
Boudouresque C F, Verlaque M. 2001a. Ecology of Paracentrotus lividus. In: Lawrence J M, ed. Edible Sea Urchins: Biology and Ecology. Amsterdam: Elsevier, 177–215
Boudouresque C F, Verlaque M. 2001b. Ecology of Paracentrotus lividus. In: Lawrence J M, ed. Edible Sea Urchins: Biology and Ecology. Amsterdam: Elsevier, 243–286
Bressan M, Marin M, Brunetti R. 1995. Influence of temperature and salinity on embryonic development of Paracentrotus lividus (Lmk, 1816). Hydrobiologia, 304(3): 175–184
Calderon 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(1): 137–151
Calderon I, Palacin C, Turon X. 2009. Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in northwest Mediterranean. Mol Ecol, 18(14): 3036–3049
Calderon I, Pita L, Brusciotti S, et al. 2012. Time and space: genetic structure of the cohorts of the common sea urchin Paracentrotus lividus in Western Mediterranean. Mar Biol, 159(1): 187–197
Cantatore P, Roberti M, Rainaldi G, et al. 1989. The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem, 264(19): 10965–10975
Calderon I, Turon X. 2010. Temporal genetic variability in the Mediterranean common sea urchin Paracentrotus lividus. Mar Ecol Prog Ser, 408: 149–159
Clark P U, Dyke A S, Shakun J D, et al. 2009. The last glacial maximum. Science, 325(5941): 710–714
Clarke K R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust Ecol, 18(1): 117–143
Collina-Girard J. 2001. L'Atlantide devant le détroit de Gibraltar? Mythe et géologie atlantis off the gibraltar strait?. Myth and geology Comptes Rendus l'Acad Sci Ser II A Earth Planet Sci, 333(4): 233–240
Dance C. 1987. Patterns of activity of the sea urchin Paracentrotus lividus in the Bay of Port-Cros (Var, France, Mediterranean). Mar Ecol, 8(2): 131–142
Davis J C. 1986. Statistics and Data Analysis in Geology. Hoboken: John Wiley and Sons, 656
Deli T, Bahles H, Said K, et al. 2015a. Patterns of genetic and morphometric diversity in the marbled crab (Pachygrapsus marmoratus, Brachyura, Grapsidae) populations across the Tunisian coast. Acta Oceanol Sinica, 34(6): 49–58
Deli T, Chatti N, Said K, et al. 2016. Concordant patterns of mtDNA and nuclear phylogeographic structure reveal Pleistocene vicariant event in the green crab Carcinus aestuarii across the Siculo-Tunisian Strait. Med Mar Sci, 17(2): 533–551
Deli T, Said K, Chatti N. 2014. Morphological differentiation among geographically close populations of the green crab Carcinus aestuarii Nardo, 1847 (Brachyura, Carcinidae) from the Tunisian coast. Crustaceana, 87(3): 257–283
Deli T, Said K, Chatti N. 2015b. Genetic differentiation among populations of the green crab Carcinus aestuarii (Nardo, 1847) (Bra chyura, Carcinidae) from the Eastern and Western Mediterranean coast of Tunisia. Acta Zool Bulg, 67(3): 327–335
Duran S, Palacin C, Becerro M A, et al. 2004. Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol, 13(11): 3317–3328
Ebert T A. 1980. Relative growth of sea urchin jaws: an example of plastic resource allocation. Bull Mar Sci, 30: 467–474
Ebert T A. 1988. Allometry, design and constraint of body components and of shape in sea urchins. J Nat Hist, 22(5): 1407–1425
Epherra L, Crespi-Abril A, Meretta P E, et al. 2015. Morphological plasticity in the Aristotle's lantern of Arbacia dufresnii (Phymosomatoida: Arbaciidae) off the Patagonian coast. Rev Biol Trop, 63: 339–351
Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3. 0): an integrated software package for population genetics data analysis. Evol Bioinform, 1: 47–50
Excoffier L, Smouse P E, Quattro J M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2): 479–491
Felsenstein J. 1989. PHYLIP-phylogeny inference package (Version 3.2). Cladistics, 5: 164–166
Fernandez C. 1996. Croissance et nutrition de Paracentrotus lividus dans le cadre d'un projet aquacole avec alimentation artificielle [dissertation]. Corse: Université de Corse
Fernandez C, Boudouresque C F. 1997. Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser, 152: 145–154
Fernandez C, Pasqualini V, Boudouresque C F, et al. 2006. Effect of an exceptional rainfall event on the sea urchin (Paracentrotus lividus) stock and seagrass distribution in a Mediterranean coastal lagoon. Estuar Coast Shelf Sci, 68(1-2): 259–270
Forcucci D, Lawrence J M. 1986. Effect of low salinity on the activity, feeding, growth and absorption efficiency of Luidia clathrata (Echinodermata: Asteroidea). Mar Biol, 92(3): 315–321
Gharbi A, Zitari-Chatti R, Van Wormhoudt A, et al. 2011. Allozyme variation and population genetic structure in the carpet shell clam Ruditapes decussatus across the Siculo-Tunisian strait. Biochem Genet, 49(11-12): 788–805
Grant W S, Spies I B, Canino M F. 2006. Biogeographic evidence for selection on mitochondrial DNA in North Pacific walleye pollock Theragra chalcogramma. J Hered, 97(6): 571–580
Guidetti P, Dulcic J. 2007. Relationships among predatory fish, sea urchins and barrens in Mediterranean rocky reefs across a latitudinal gradient. Mar Environ Res, 63(2): 168–184
Guidetti P, Terlizzi A, Boero F. 2004. Effects of the edible sea urchin, Paracentrotus lividus, fishery along the Apulian rocky coast (SE Italy, Mediterranean Sea). Fish Res, 66(2-3): 287–297
Hagen N T. 2008. Enlarged lantern size in similar-sized, sympatric, sibling species of Strongylocentrotid sea urchins: from phenotypic accommodation to functional adaptation for durophagy. Mar Biol, 153(5): 907–924
Hammer Ø, Harper D A T, Ryan P D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron, 4(1): 1–9
Hampton K R, Hopkins M J, McNamara J C, et al. 2014. Intraspecific variation in carapace morphology among fiddler crabs (Genus Uca) from the Atlantic coast of Brazil. Aquat Biol, 20(1): 53–67
Hedgecock D, Barber P H, Edmands S. 2007. Genetic approaches to measuring connectivity. Oceanography, 20: 70–79
Hellberg M E. 1996. Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution, 50(3): 1167–1175
Hopkins M J, Thurman C L. 2010. The geographic structure of morphological variation in eight species of fiddler crabs (Ocypodidae: genus Uca) from the eastern United States and Mexico. Biol J Linn Soc, 100(1): 248–270
Iuri V, Patti F P, Procaccini G. 2007. Phylogeography of the sea urchin Paracentrotus lividus (Lamarck) (Echinodermata: Echinoidea): first insights from the South Tyrrhenian Sea. Hydrobiologia, 580(1): 77–84
Johnson R A, Wichern D W. 1998. Applied Multivariate Statistical Analysis. 4th ed. Englewood Cliffs, USA: Prentice Hall, Inc, 816
Kaouèche M, Bahri-Sfar L, Gonzalez-Wangüemert M, et al. 2011. Allozyme and mtDNA variation of white seabream Diplodus sargus populations in a transition area between western and eastern Mediterranean basins (Siculo-Tunisian Strait). Afr J Mar Sci, 33(1): 79–90
Launey S, Ledu C, Boudry P, et al. 2002. Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. J Hered, 93(5): 331–351
Lawrence J M, Agatsuma Y. 2001. The ecology of Tripneustes. Developments in Aquac Fish Sci, 32: 395–413
Lessios H A, Kessing B D, Pearse J S. 2001. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution, 55(5): 955–975
Lopéz S, Turon X, Montero E, et al. 1998. Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea). Interannual variability and plankton-benthos coupling. Mar Ecol Prog Ser, 172: 239–251
Lozano J, Galera J, Lopez S, et al. 1995. Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser, 122: 179–191
Lumingas L J L. 1994. La plasticité chez l'oursin Sphaerechinus granulans en rade de Brest (Bretagne, France) [dissertation]. Brest, France: Université de Bretagne Occidentale
Maggs C A, Castilho R, Foltz D, et al. 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89(sp11): S108–S122
Maltagliati F, Di Giuseppe G, Barbieri M, et al. 2010. Phylogeography and genetic structure of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) inferred from the mitochondrial cytochrome b gene. Biol J Linn Soc, 100(4): 910–923
McClanahan T R, Nugues M, Mwachireya S. 1994. Fish and sea urchin herbivory and competition in Kenyan coral reef lagoons: the role of reef management. J Exp Mar Biol Ecol, 184(2): 237–254
McElroy D, Moran P, Bermingham E, et al. 1992. REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data. J Hered, 83(2): 157–158
Mejri R, Lo Brutto S, Hassine O K B, et al. 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(2): 596–601
Middleton D A J, Gurney W S C, Gage J D. 1998. Grow th and energy allocation in the deep-sea urchin Echinus affinis. Biol J Linn Soc, 64(3): 315–336
Mojetta A, Ghisotti A. 1996. Flore et faune de la Méditerranée. Alibert-Kouraguine D, trans. Paris: Solar Publication, 318
Nei M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press, 512
Nei M, Tajima F. 1981. DNA polymorphism detectable by restriction endonucleases. Genetics, 97(1): 145–163
Nikula R, Väinölä R. 2003. Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol, 143(2): 339–350
Pedrotti M L. 1993. Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. J Mar Biol Assoc U K, 73(3): 513–530
Penant G, Aurelle D, Feral J P, et al. 2013. Planktonic larvae do not ensure gene flow in the edible sea urchin Paracentrotus lividus. Mar Ecol Prog Ser, 480: 155–170
Pérès J M. 1985. History of the Mediterranean biota and the colonization of the depths. In: Margalef R, ed. Western Mediterranean. Oxford: Pergamon, 198–232
Pinardi N, Masetti E. 2000. Variability of the large scale general circulation of the Mediterranean Sea from observations and modelling: a review. Palaeogeogr Palaeoclimatol Palaeoecol, 158 (3-4): 153–174
Quesada H, Beynon C M, Skibinski D O F. 1995. A mitochondrial DNA discontinuity in the mussel Mytilus Galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol, 12(3): 521–524
Quignard J P. 1978. La Méditerranée creuset ichthyologique. Boll Zool, 45(S2): 23–36
Régis M B. 1979. Analyse des fluctuations des indices physiologiques chez deux échinoides (Paracentrotus lividus (LmK) et Arbacia lixula L.) du golfe de Marseille. Téthys, 9(2): 167–181
Rice W R. 1989. Analyzing tables of statistical tests. Evolution, 43(1): 223–225
Rizzo C, Cammarata M, Di Carlo M, et al. 2009. RAPD profiles distinguish Paracentrotus lividus populations living in a stressing environment (Amvrakikos Gulf, Greece). Russ J Genet, 45(4): 499–503
Roff D A, Bentzen P. 1989. The statistical analysis of mitochondrial DNA polymorphisms: X2 and the problem of small samples. Mol Biol Evol, 6(5): 539–545
Rozen S, Skaletsky H J. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S A, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, New Jersey: Humana Press, 365–386
Sala E, Zabala M. 1996. Fish predation and the structure of the sea urchin Paracentrotus lividus populations in the NW Mediterranean. Mar Ecol Prog Ser, 140: 71–81
Sammon J W. 1969. A nonlinear mapping for data structure analysis. IEEE Trans Comput, C-18(5): 401–409
Schluter D. 2000. Ecological character displacement in adaptive radiation. Am Nat, 156(S4): S4–S16
Sellem F, Guillou M. 2007. Reproductive biology of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats of northern Tunisia (south-east Mediterranean). J Mar Biol Assoc U K, 87(3): 763–767
Serena F. 2005. Field identification guide to the sharks and rays of the Mediterranean and Black Sea. FAO Species Identification Guide for Fishery Purposes. Rome: FAO, 97
Solé-Cava A M, Thorpe J P. 1991. High levels of genetic variation in natural populations of marine lower invertebrates. Biol J Linn Soc, 44(1): 65–80
Soualili D L. 2008. Les populations naturelles d'oursins: un outil évaluateur de l'état de santé de la d'Alger [dissertation]. Algiers, Algeria: Université des Sciences et de la Technologie Houari Boumediene
StatSoft, Inc. 1993. STATISTICA (data analysis software system: for the windows operating system reference for statistical procedures), version 4.5. www.statsoft.com
Thiede J. 1978. A glacial Mediterranean. Nature, 276(5689): 680–683
Turon X, Giribet G, Lopez S, et al. 1995. Growth and population structure of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser, 122: 193–204
Venables W N, Ripley B D. 2002. Modern Applied Statistics with S. 4th ed. New York, USA: Springer-Verlag, 495
Wangensteen O S, Dupont S, Casties I, et al. 2013. Some like it hot: temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula. J Exp Mar Biol Ecol, 449: 304–311
Wright S. 1950. Genetical structure of populations. Nature, 166(4215): 247–249
Zitari-Chatti R, Chatti N, Elouaer A, et al. 2008. Genetic variation and population structure of the caramote prawn Penaeus kerathurus (Forskäl) from the eastern and western Mediterranean coasts in Tunisia. Aquac Res, 39(1): 70–76
Zitari-Chatti R, Chatti N, Fulgione D, et al. 2009. Mitochondrial DNA variation in the caramote prawn Penaeus (Melicertus) kerathurus across a transition zone in the Mediterranean Sea. Genetica, 136(3): 439–447
Acknowledgements
The authors are grateful to everybody who assisted in this work. Specifically, the authors thank colleagues from Algeria (Lamia Boudechiche) and Libya (Daou Haddoud) for their help with sea urchins sampling. Special thanks are also extended to two anonymous reviewers for their very helpful and interesting comments and suggestions to improve the manuscript quality.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Deli, T., Ben Attia, M.H., Zitari-Chatti, R. et al. Genetic and morphological divergence in the purple sea urchin Paracentrotus lividus (Echinodermata, Echinoidea) across the African Mediterranean coast. Acta Oceanol. Sin. 36, 52–66 (2017). https://doi.org/10.1007/s13131-017-1090-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13131-017-1090-3