Marine Biodiversity

, Volume 49, Issue 2, pp 603–620 | Cite as

High genetic connectivity among morphologically differentiated populations of the black sea urchin Arbacia lixula (Echinoidea: Arbacioida) across the central African Mediterranean coast

  • Temim DeliEmail author
  • Ahmed Ben Mohamed
  • Mohamed Hbib Ben Attia
  • Rym Zitari-Chatti
  • Khaled Said
  • Noureddine Chatti
Original Paper


The present study represents the first population structure analysis of the black sea urchin Arbacia lixula across part of its African Mediterranean distribution range, the Tunisian coast. This location is appropriate for the study of biogeographical processes given the presence of a well-known discontinuous biogeographic area (the Siculo-Tunisian Strait). Patterns of morphological and genetic variation in this highly dispersive echinoid species were assessed among its populations from the western and eastern Mediterranean coasts of Tunisia. A total of 109 specimens from six sites were collected and examined for morphometric variability in seven morphometric traits. Concordant results, inferred from CDA analyses, pairwise NPMANOVA comparisons and MDS plot, showed significant inter-population differences in the measured traits among the studied populations. In addition, UPGMA clustering and discriminant/Hotelling analysis enabled the delineation of two morphologically differentiated groups assigned to the western and eastern Mediterranean basins. SIMPER analysis showed that total dry weight and test diameter were major contributors to the morphometric separation between locations and among groups. Despite the extensive morphological variation found in A. lixula, genetic analysis of the mitochondrial COI marker recovered only a single evolutionary lineage and showed a lack of population structure as inferred from the results of one-level AMOVA and pairwise comparisons of genetic differentiation. Possible explanations for this genetic pattern are discussed. Notably, the lack of COI divergence patterns, highlighted by shallow genealogy associated with high haplotype diversity and low nucleotide diversity, together with a recent demographic expansion event retrieved from mismatch distribution and BSP analysis could be considered a residual effect of a recent evolutionary history of the species in the Mediterranean.


Arbacia lixula Tunisian coast Morphological differentiation COI Genetic homogeneity Demographic expansion 



The authors would like to thank three anonymous reviewers for their very helpful and interesting comments and suggestions that improved the quality of the manuscript.


  1. Alcoverro T, Mariani S (2002) Effects of sea urchin grazing on seagrass (Thallasoma ciliatum) beds of a Kenyan lagoon. Mar Ecol Prog Ser 226:255–263Google Scholar
  2. Anastasiadou C, Leonardos ID (2008) Morphological variation among populations of Atyaephyra desmarestii (millet, 1831) (Decapoda: Caridea: Atyidae) from freshwater habitats of northwestern Greece. J Crustacean Biol 28(2):240–247Google Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Anderson MJ (2005) Permanova-Permutational multivariate analysis of variance. Department of Statistics, University of Auckland, AucklandGoogle Scholar
  5. Arakaki Y, Uehara T, Fagoonee I (1998) Comparative studies of the genus Echinometra from Okinawa and Mauritius. Zool Sci 15:159–168Google Scholar
  6. Arculeo M, Brutto SL, Pancucci MP, Cammarata M, Parrinello N (1998) Allozyme similarity in two morphologically distinguishable populations of Paracentrotus lividus (Echinodermata) from distinct areas of the Mediterranean coast. J Mar Biol Assoc UK 78:231–238Google Scholar
  7. Arnaud-Haond S, Diaz Almela E, Teixeira S (2007) Vicariance patterns in the Mediterranean Sea: east-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J Biogeogr 14:963–976Google Scholar
  8. Avise JC (2000) Phylogeography: the history and formation of species. MA. Harvard University Press, CambridgeGoogle Scholar
  9. 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 267:929–935Google Scholar
  10. Balisco RAT (2015) Notes on the gracious sea urchin Tripneustes gratilla (Echinodermata: Echinoidea) in Pag-asa Island, Kalayaan, Palawan, Philippines. The Palawan. Scientist 7:27–35Google Scholar
  11. Bardaji T, Goy JL, Zazo C, Hillaire-Marcel C, Dabrio CJ, Cabero A, Ghaleb B, Silva PG, Lario J (2009) Sea level and climate changes during OIS 5e in the western Mediterranean. Geomorphology 104:22–37Google Scholar
  12. Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past. Amer Zool 39:131–145Google Scholar
  13. 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 51:411–440Google Scholar
  14. Black R, Codd C, Hebbert D, Vink S, Burt J (1984) The functional significance of the relative size of Aristotle’s lantern in the sea urchin Echinometra mathaei (de Blainville). J Exp Mar Biol Ecol 77:81–97Google Scholar
  15. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45Google Scholar
  16. Borrero-Pérez GH, Gonzalez-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 20:1964–1975Google Scholar
  17. Borsa P, Blanquer A, Berrebi P (1997) Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Mar Biol 129:233–246Google Scholar
  18. Bulleri F, Benedetti-Cecchi L, Cinelli F (1999) Grazing by the sea urchins Arbacia lixula L. and Paracentrotus lividus Lam. in the Northwest Mediterranean. J Exp Mar Biol Ecol 241:81–95Google Scholar
  19. 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 154:137–151Google Scholar
  20. Chatti N, Zitari-Chatti R, Attia MH, Ben Khadra Y, Said K (2012) Very low mitochondrial diversity and genetic homogeneity in the starfish Echinaster sepositus along the Tunisian coast. Biochem Genet 50:45–51Google Scholar
  21. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143Google Scholar
  22. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660Google Scholar
  23. Cobb J, Lawrence JM (2005) Diets and coexistence of the sea urchin Lytechinus variegatus and Arbacia puntulata (Echinodermata) along the central Florida gulf coast. Mar Ecol Prog Ser 205:171–182Google Scholar
  24. Davis JC (1986) Statistics and data analysis in geology. John Wiley and SonsGoogle Scholar
  25. De Giorgi C, Martiradonna A, Lanave C, Saccone C (1996) Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Mol Phylogenet Evol 5:323–332Google Scholar
  26. Deli T, Bahles H, Said K, Chatti N (2015a) Patterns of genetic and morphometric diversity in the marbled crab (Pachygrapsus marmoratus, Brachyura, Grapsidae) populations across the Tunisian coast. Acta Oceanol Sini 34(6):49–58Google Scholar
  27. Deli T, Ben Attia MH, Zitari-Chatti R, Said K, Chatti N (2017) Genetic and morphological divergence in the purple sea urchin Paracentrotus lividus (Echinodermata, Echinoidea) across the African Mediterranean coast. Acta Oceanol Sini 36(12):52–66 Google Scholar
  28. 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):533–551Google Scholar
  29. 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):471–487Google Scholar
  30. 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):257–283Google Scholar
  31. Deli T, Said K, Chatti N (2015b) Genetic differentiation among populations of the green crab Carcinus aestuarii (Brachyura, Carcinidae) from the eastern and western Mediterranean coasts of Tunisia. Acta Zool Bulg 67(3):327–335Google Scholar
  32. Dix TG (1970) Biology of Evechinus chloroticus (Echinoidea: Echinometridae) from different localities. New Zeal J Mar Fresh Res 4(3):267–277Google Scholar
  33. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192Google Scholar
  34. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973Google Scholar
  35. Duda TF, Terbio M, Chen G, Phillips S, Olenzek AM, Chang D, Morris DW (2012) Patterns of population structure and historical demography of Conus species in the tropical Pacific. Amer Malac Bull 30:175–187Google Scholar
  36. Duran S, Palacin 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 13:3317–3328Google Scholar
  37. Ebert TA (1980) Relative growth of sea urchin jaws: an example of plastic resource allocation. Bull Mar Sci 30:467–474Google Scholar
  38. Ebert TA (1982) Longevity, life history, and relative body wall size in sea urchins. Ecol Monogr 45:353–394Google Scholar
  39. Ebert TA (1988) Allometry, design and constraint of body components and of shape in sea urchins. J Nat Hist 22:1407–1425Google Scholar
  40. Eckman JE (1996) Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. J Exp Mar Biol Ecol 200:207–237Google Scholar
  41. Epherra L, Crespi-Abril A, Meretta PE, Maximiliano Cledón M, Enrique Mario Morsan EM, Rubilar T (2015) Morphological plasticity in the Aristotle’s lantern of Arbacia dufresnii (Phymosomatoida: Arbaciidae) off the Patagonian coast. Rev Biol Trop 63:339–351Google Scholar
  42. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864Google Scholar
  43. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  44. 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 131:479–491Google Scholar
  45. Fenaux L (1968) Maturation des gonades et cycle saisonnier des larves chez A. lixula, P. lividus et P. microtuberculatus à Villefranche-Sur-Mer. Vie Milieu A Biol Ma 19:1–52Google Scholar
  46. Fernandez C (1996) Croissance et nutrition de Paracentrotus lividus dans le cadre d'un projet aquacole avec alimentation artificielle. PhD thesis, Université de CorseGoogle Scholar
  47. Fernandez C, Boudouresque C-F (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152:145–154Google Scholar
  48. Fernandez C, Boudouresque C-F (2000) Nutrition of the sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) fed different artificial food. Mar Ecol Prog Ser 204:131–141Google Scholar
  49. Forcucci D, Lawrence JM (1986) Effect of low salinity on the activity, feeding, growth and absorption efficiency of Luidia clathrata (Echinodermata: Asteroidea). Mar Biol 92:315–321Google Scholar
  50. Francour P, Boudouresque C-F, Harmelin JG, Harmelin-Vivien ML, Quignard JP (1994) Are the Mediterranean waters becoming warmer? Information from biological indicators. Mar Pollut Bull 28:523–526Google Scholar
  51. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genet Soc Amer 147:915–925Google Scholar
  52. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF (2009) The influence of oceanographic fronts and early-life history traits on connectivity among littoral fish species. Proc Natl Acad Sci U S A 106:1473–1478Google Scholar
  53. Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626Google Scholar
  54. Gerlach G, Atema J, Kingsford M, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci U S A 104:858–863Google Scholar
  55. Gianguzza P, Agnetta D, Bonaviri C, Di Trapani F, Visconti G, Gianguzza F, Riggio S (2011) The rise of thermophilic sea urchins and the expansion of barren grounds in the Mediterranean Sea. Chem Ecol 27:129–134Google Scholar
  56. Guidetti P, Fraschetti S, Terlizzi A, Boero F (2003) Distribution patterns of sea urchins and barrens in shallow Mediterranean rocky reefs impacted by the illegal fishery of the rock-boring mollusc Lithophaga lithophaga. Mar Biol 143:1135–1142Google Scholar
  57. Hagen NT (2008) Enlarged lantern size in similar-sized, sympatric, sibling species of Strongylocentrotid sea urchins: from phenotypic accommodation to functional adaptation for durophagy. Mar Biol 153:907–924Google Scholar
  58. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95 / 98 / NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  59. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9Google Scholar
  60. Hampton KR, Hopkins MJ, McNamara JC, Thurman CL (2014) Intraspecific variation in carapace morphology among fiddler crabs (genus Uca) from the Atlantic coast of Brazil. Aquatic Biol 20:53–67Google Scholar
  61. Harmelin JG, Hereu B, De Maisonnave LM, Teixidor N, Domínguez L, Zabala M (1995) Indicateurs de biodiversité en milieu marin: les échinodermes. Fluctuations temporelles des peuplements d’échinodermes à Port-Cros. Comparaison entre les années 1982–84 et 1993–95. Internal Report. Port Cros National ParkGoogle Scholar
  62. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66(4):591–600Google Scholar
  63. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362Google Scholar
  64. Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull Mar Sci 39:550–565Google Scholar
  65. Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol Syst 40:291–310Google Scholar
  66. Hilbish TJ (1996) Population genetics of marine species: the interaction of natural selection and historically differentiated populations. J Exp Mar Biol Ecol 200:67–83Google Scholar
  67. Hopkins MJ, Thurman CL (2010) The geographic structure of morphological variation of eight species of fiddler crabs (Ocypodidae: genus Uca) from the eastern United States and Mexico. Biol J Linnean Soc 100:248–270Google Scholar
  68. 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 1–44Google Scholar
  69. Johnson RA, Wichern DW (1998) Applied multivariate statistical analysis, Fourth edn. Prentice-Hall, Inc, USA, 816 ppGoogle Scholar
  70. Kaouèche M, Bahri-Sfara L, González-Wangüemert M, Pérez-Ruzafa Á, Ben Hassine OK (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 Marine Sci 33(1):79–90Google Scholar
  71. Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern Pacific rocky intertidal community. PLoS One 5(1):e8594Google Scholar
  72. Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576Google Scholar
  73. Lawrence JM, Agatsuma Y (2007) The ecology of Tripneustes. Dev Aquacult Fish Sci 37:499–520Google Scholar
  74. Lessios HA (1981) Divergence in allopatry: molecular and morphological differentiation between sea urchins separated by the isthmus of Panama. Evolution 35:618–634Google Scholar
  75. Lessios HA (2009) Speciation in sea urchins. In: Harris L, Böttger S, Walker C, Lesser M (eds) Echinoderms: Durham proceedings of the 12th international echinoderm conference, 7–11 august 2006, Durham, New Hampshire, USA. CRC Press, London, pp 91–101Google Scholar
  76. Lessios HA (2011) Speciation genes in free-spawning marine invertebrates. Integr Comp Biol 51:456–465Google Scholar
  77. Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036Google Scholar
  78. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975Google Scholar
  79. Lessios HA, Lockhart S, Collin R, Sotil G, Sanchez-Jerez P, Zigler KS, Perez AF, Garrido MJ, Geyer LB, Bernardi G, Vacquier VD, Haroun R, Kessing BD (2012) Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution. Mol Ecol 21:130–144Google Scholar
  80. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452Google Scholar
  81. Li WH (1977) Distribution of nucleotide differences between two randomly chosen cistrons in a finite population. Genetics 85:331–337Google Scholar
  82. Lumnigas LJL (1994) La plasticité chez l'oursin Sphaerechinus granularis en rade de Brest (Bretagne, France). PhD thesis, Université de Bretagne OccidentaleGoogle Scholar
  83. Maltagliati F, Di Giuseppe G, Barbieri M, Castelli A, Dini F (2010) Phylogeography and genetic structure of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) inferred from the mitochondrial cytochrome b gene. Biol J Linnean Soc 100:910–923Google Scholar
  84. McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400Google Scholar
  85. Meiri S (2010) Length-weight allometries in lizards. J Zool 3:218–226Google Scholar
  86. 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 53:596–601Google Scholar
  87. Middleton DAJ, Gurney WSC, Gage JD (1998) Growth and energy allocation in the deep-sea urchin Echinus affinis. Biol J Linnean Soc 64:315–336Google Scholar
  88. Michaud JE, Echternacht AC (1995) Geographic variation in the life history of the lizard Anolis carolinensis and support for the pelvic constraint model. J Herpetol 29:86–97Google Scholar
  89. Mortensen T (1935) A monograph of the Echinoidea. II. Bothriocidaroida, Melonechinoida, lepidocentroida, and Stirodonta. Copenhagen & London: Reitzel & Oxford Univ. Press. 647 pGoogle Scholar
  90. Muths D, Jollivet D, Gentil F, Davoult D (2009) Largescale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquatic Biol 5:117–132Google Scholar
  91. Nei M (1987) Molecular Euolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  92. Nikula R, Vainola R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the eastern Mediterranean. Mar Biol 143:339–350Google Scholar
  93. Oliver TA, Garfield DA, Manier MK, Haygood R, Wray GA, Palumbi SR (2010) Whole genome positive selection and habitat-driven evolution in a shallow and a deep-sea urchin. Genome Biol Evol 2:800–814Google Scholar
  94. Palacin C, Turon X, Ballesteros M, Giribet G, Lopez S (1998) Stock evaluation of three littoral echinoid species on the Catalan coast (north-western Mediterranean). Mar Ecol 19:163–177Google Scholar
  95. Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L., eds. Larval Ecology. CRC Press, pp. 369–386Google Scholar
  96. Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517Google Scholar
  97. Patarnello T, Volckaert FAM, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444Google Scholar
  98. Pearse JS (2006) Ecological role of purple sea urchins. Science 314:940–941Google Scholar
  99. Pedrotti ML (1993) Spatial and temporal distribution and recruitment of echinoderm larvae in the Ligurian Sea. J Mar Biol Assoc U K 73:513–530Google Scholar
  100. Penant G, Aurelle D, Feral JP, Chenuil A (2013) Planktonic larvae do not ensure gene flow in the edible sea urchin Paracentrotus lividus. Mar Ecol Prog Ser 480:155–170Google Scholar
  101. Pérez-Portela R, Villamor A, Almada VC (2010) Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western Mediterranean. Mar Biol 157:2015–2028Google Scholar
  102. Pespeni MH, Barney BT, Palumbi SR (2013) Differences in the regulation of growth and biomineralization genes revealed through long-term common-garden acclimation and experimental genomics in the purple sea urchin. Evolution (special section).
  103. 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 158:153–174Google Scholar
  104. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818Google Scholar
  105. Posada D, Crandall KA (2001) Selecting the best-fit model of nucleotide substitution. Syst Biol 50:580–601Google Scholar
  106. Privitera D, Noli M, Falugi C, Chiantore M (2011) Benthic assemblages and temperature effects on Paracentrotus lividus and Arbacia lixula larvae and settlement. J Exp Mar Biol Ecol 407:6–11Google Scholar
  107. Pujolar JM, Pogson GH (2011) Positive Darwinian selection in gamete recognition proteins of Strongylocentrotus sea urchins. Mol Ecol 20:4968–4982Google Scholar
  108. Quesada H, Beynon CM, Skibinski DOF (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: Pleistocene vicariance biogeography and secondary intergradations. Mol Biol Evol 12:521–524Google Scholar
  109. Rambaut A, Drummond AJ (2007) Tracer v 1.4.8. Institute of Evolutionary Biology, University of Edinburgh, Available from: http//
  110. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100Google Scholar
  111. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  112. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Misener S, Krawetz SA (eds) Bioinformatics methods and protocols, vol 132. Humana Press, New Jersey, pp 365–386Google Scholar
  113. Sala E, Boudouresque CF, Harmelin-Vivien ML (1998) Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82:425–439Google Scholar
  114. Sammon J (1969) A nonlinear mapping for data structure analysis. IEEE Trans Comput 18(5):401–409Google Scholar
  115. Sanford E, Kelly MW (2011) Local adaptation in the sea. Annu Rev Mar Sci 3:509–535Google Scholar
  116. Selkoe KA, Watson JR, White C, Ben Horin T, Iacchei M, Mitarai S (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mole. Ecol 19:3708–3726Google Scholar
  117. 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. Rome: FAO, 97 ppGoogle Scholar
  118. 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 87:651–701Google Scholar
  119. Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Int J Org Evolution 43:1349–1368Google Scholar
  120. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA 731 sequences in stable and exponentially growing populations. Genetics 129:555–562Google Scholar
  121. Slatkin M, Maddison WP (1990) Detecting isolation by distance using phylogenies of genes. Genetics 126:249–260Google Scholar
  122. Sponer R, Deheyn D, Roy MS (2001) Large genetic distances within a population of Amphipholis squamata (Echinodermata; Ophiuroidea) do not support colour varieties as sibling species. Mar Ecol Prog Ser 219:169–175Google Scholar
  123. StatSoft Inc (1993) STATISTICA (data analysis software system: for the windows operating system reference for statistical procedures), version 4.5. Computer program
  124. Stefanini G (1911) Di alcune Arbacia fossili. Riv Ital Paleontol 17:51–52Google Scholar
  125. Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105:437–460Google Scholar
  126. Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics Soc Amer 123:597–601Google Scholar
  127. Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285Google Scholar
  128. 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 28:2731–2739Google Scholar
  129. 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 132:619–633Google Scholar
  130. Thiede J (1978) A glacial Mediterranean. Nature 276:680–683Google Scholar
  131. Tortonese E (1965) Echinodermata. Fauna d’Italia vol. VI. Bologna: Calderini. 422 pGoogle Scholar
  132. Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth edn. Springer-Verlag, New York, p 495Google Scholar
  133. Wangensteen OS, Dupont S, Casties I, Turon X, Palacin C (2013) Some like it hot: temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula. J Exp Mar Biol Ecol 449:304–311Google Scholar
  134. Wangensteen OS, Turon X, Garcia-Cisneros A, Recasens M, Romero J, Palacin C (2011) A wolf in sheep’s clothing: carnivory in dominant sea urchins in the Mediterranean. Mar Ecol Prog Ser 441:117–128Google Scholar
  135. Wangensteen OS, Turon X, Pérez-Portela R, Palacin C (2012) Natural or naturalized? Phylogeography suggests that the abundant sea urchin Arbacia lixula is a recent colonizer of the Mediterranean. PLoS One 7(9):e45067Google Scholar
  136. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450Google Scholar
  137. Waters JM, Roy MS (2004) Phylogeography of a high-dispersal New Zealand sea-star: does upwelling block gene-flow? Mol Ecol 13:2797–2806Google Scholar
  138. Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12Google Scholar
  139. Wing SR, Largier JL, Botsford LW, Quinn JF (1995) Settlement and transport of benthic invertebrates in an intermittent upwelling zone. Limnol Oceanogr 40:316–329Google Scholar
  140. Zitari-Chatti R, Chatti N, Elouaer A, Said K (2008) Genetic variation and population structure of the caramote prawn Penaeus kerathurus (Forskal) from the eastern and western Mediterranean coasts in Tunisia. Aquac Res 39:70–76Google Scholar
  141. Zitari-Chatti R, Chatti N, Fulgione D, Gaiazza 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 136:439–447Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Temim Deli
    • 1
    Email author
  • Ahmed Ben Mohamed
    • 1
  • Mohamed Hbib Ben Attia
    • 1
  • Rym Zitari-Chatti
    • 1
  • Khaled Said
    • 1
  • Noureddine Chatti
    • 1
  1. 1.Laboratory of Genetics, Biodiversity and Enhancement of Bioresources (LR11ES41)University of Monastir, Higher Institute of Biotechnology of MonastirMonastirTunisia

Personalised recommendations