Marine Biology

, Volume 149, Issue 3, pp 465–481 | Cite as

Phylogeographic patterns of the mysid Mesopodopsis slabberi (Crustacea, Mysida) in Western Europe: evidence for high molecular diversity and cryptic speciation

  • Thomas RemerieEmail author
  • Tine Bourgois
  • Danny Peelaers
  • Andy Vierstraete
  • Jacques Vanfleteren
  • Ann Vanreusel
Research Article


The phylogeographic patterns among populations of Mesopodopsis slabberi (Crustacea, Mysida), an ecological important mysid species of marine and estuarine habitats, were analysed by means of DNA sequencing of a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) and the 16S ribosomal RNA genes. Samples of M. slabberi collected from five Atlantic and two Western Mediterranean populations were investigated. Very high levels of within-population molecular diversity were observed in all samples (mean h=0.807 and π=0.0083), with exception of the Mediterranean Ebro population which contained only one haplotype. Differentiation among populations was high, and a clear phylogeographic break was observed between the Atlantic and Mediterranean populations. Moreover, a strong differentiation was detected between both populations in the Western Mediterranean Sea (Alicante and Ebro delta), while two divergent lineages occurred in sympatry within the Atlantic Mondego estuary. The high congruence between both the COI and 16S rRNA sequence data, the reciprocal monophyly of the different mitochondrial clades and the levels of nucleotide divergence between them suggest the presence of a complex of cryptic species within M. slabberi. Estimations of divergence time between the different mitochondrial lineages indicate that a split occurred during the late Miocene/early Pliocene. Such a divergence could be concordant with vicariant events during sea-level drops within the Mediterranean region at that time. However, within the Mediterranean Sea, the potential of divergence through ecological diversification cannot be ruled out.


Ebro Delta Messinian Salinity Crisis Mysid Species Mondego Estuary Shimodaira Hasegawa Test 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research is supported by the FWO project G029200, the GOA BOF project (1205398) ‘Biodiversity of marine benthic communities along ecological gradients’ from Ghent University (Flemish Government of Education) and the TROPHOS project of the Belgian Federal Science Policy Office (contract No. EV/02/25A). We would like to thank J.-C. Dauvin, A. M. Sardo, M. Cunha, M. R. Pastorinho P. D. Moyano, C. Barbera, C. Ribera and T. Wooldridge for their help with collecting and providing samples.


  1. Avise JC, Ball RM, Arnold J (1988) Current versus historical population sizes in vertebrate species with high gene flow: a comparison based on mitochondrial DNA lineages and inbreeding theory for neutral mutations. Mol Biol Evol 5:331–344PubMedGoogle Scholar
  2. Azeiteiro UMM, Jesus L, Marques JC (1999) Distribution, population dynamics, and production of the suprabenthic mysid Mesopodopsis slabberi in the Mondego estuary, Portugal. J Crust Biol 19:498–509CrossRefGoogle Scholar
  3. Bacescu M (1940) Les Mysidacés des eaux Roumaines (Etude taxonomique, morphologique, bio-géographique et biologique). Ann Sci Univ Jassy 26:453–804Google Scholar
  4. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic–Mediterranean divide. J Evol Biol 16:1149–1158CrossRefGoogle Scholar
  5. Beyst B, Buysse D, Dewicke A, Mees J (2001) Surf zone hyperbenthos of Belgian sandy beaches: seasonal patterns. Estuar Coast Shelf Sci 53:877–895CrossRefGoogle Scholar
  6. Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952CrossRefGoogle Scholar
  7. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefGoogle Scholar
  8. Borsa P, Naciri M, Bahri L, Chikhi L, Garcia de Leon FJ, Kotoulas G, Bonhomme F (1997) Zoogéographie infraspecifique de la mer Méditerranée. Analyse des donnees genetiques populationnelles sur seize espèces Atlanto-Mediterraneennes (Poissons et Invertébrés). Vie Milieu 47:295–305Google Scholar
  9. Bremer JR, Mejuto J, Baker AJ (1995) Mitochondrial DNA control region sequences indicate extensive mixing of swordfish (Xiphias gladius L.) populations in the Atlantic ocean. Can J Fish Aquat Sci 52:1720–1732CrossRefGoogle Scholar
  10. Bucklin A, Wiebe PH (1998) Low mitochondrial diversity and small effective population sizes on the copepods Calanus finmarchicus and Nannocalanus minor: possible impact of climate variation during recent glaciation. J Hered 89:383–392CrossRefGoogle Scholar
  11. Bucklin A, Frost BW, Kocher TD (1995) Molecular systematics of six Calanus and three Metridia species (Calanoida: Copepoda). Mar Biol 121:655–664CrossRefGoogle Scholar
  12. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol 23:313–371Google Scholar
  13. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  14. Casu M, Curini-Galletti M (2004) Sibling species in interstitial flatworms: a case study using Monocelis lineta (Proseriata: Monocelididae). Mar Biol 145:669–679Google Scholar
  15. Cognetti G (1994) Colonization of brackish waters. Mar Pollut Bull 28:583–586CrossRefGoogle Scholar
  16. Cognetti G, Maltagliati F (2000) Biodiversity and adaptive mechanisms in brackish water fauna. Mar Pollut Bull 40:7–14CrossRefGoogle Scholar
  17. Cognetti G, Maltagliati F (2004) Strategies of genetic biodiversity conservation in the marine environment. Mar Pollut Bull 48:811–812CrossRefGoogle Scholar
  18. Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969PubMedPubMedCentralGoogle Scholar
  19. Cunha MR, Moreira MH, Sorbe JC (2000) Diamysis bahirensis: a mysid species new to the Portuguese fauna and first record from the west European coast. Crustac Issues 12:139–152Google Scholar
  20. Dando PR, Southward AJ (1981) Existence of ‘Atlantic’ and ‘Mediterranean’ forms of Chthamalus montagui (Crustacea, Cirripedia) in the western Mediterranean. Mar Biol Lett 2:239–248Google Scholar
  21. Deprez T, Vanden Berghe E, Vincx M (2004) NeMys: a multidisciplenary biological information system. In: Vanden Berghe E, Brown M, Costello MJ, Heip C, Levitus S, Pissierssens P (eds) Proceedings of ‘The Colour of Ocean Data’ Symposium, Brussels, 25–27 November 2002, IOC Workshop Reports 188 (UNESCO, Paris), pp 57–63Google Scholar
  22. Dewicke A, Cattrijsse A, Mees J, Vincx M (2003) Spatial patterns of the hyperbenthos of subtidal sandbanks in the southern North Sea. J Sea Res 49:27–45CrossRefGoogle Scholar
  23. Doebeli M, Dieckmann U (2003) Speciation along environmental gradients. Nature 421:259–264CrossRefGoogle Scholar
  24. Duggen S, Hoernie K, van den Bogaard P, Rupke L, Phipps Morgan J (2003) Deep roots of the Messinian salinity crisis. Nature 422:602–605CrossRefGoogle Scholar
  25. Duran S, Giribet G, Turon X (2004a) Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea. Mol Ecol 13:109–122CrossRefGoogle Scholar
  26. Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004b) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328CrossRefGoogle Scholar
  27. Excoffier L, Smouse P, Quattro J (1992) Analyses of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  28. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  29. 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 3:294–297Google Scholar
  30. Glenn TC, Stephan W, Braun MJ (1999) Effects of a population bottleneck on whooping crane mitochondrial DNA variation. Conserv Biol 13:1097–1107CrossRefGoogle Scholar
  31. Goldman N, Anderson JP, Rodrigo AG (2000) Likelihood-based tests of topologies in phylogenetics. Sys Biol 49:652–670CrossRefGoogle Scholar
  32. Gomoiu MT (1978) Quantitative data concerning the distribution and ecology of Mesopodopsis slabberi (van Beneden) at the Danube River mouths area. Cercet Mar 11:103–112Google Scholar
  33. Greenwood JG, Jones MB, Greenwood J (1989) Salinity effects on brood maturation on the mysid crustacean Mesopodopsis slabberi. J Mar Biol Assoc UK 69:683–694CrossRefGoogle Scholar
  34. Gysels ES, Hellemans B, Pampoulie C, Volckaert FAM (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the Mediterranean and the North Sea. Mol Ecol 13:403–417CrossRefGoogle Scholar
  35. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 122–134Google Scholar
  36. Holland BS, Dawson MN, Crow GL (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128CrossRefGoogle Scholar
  37. Hostens K, Mees J (1999) The mysid-feeding guild of demersal fishes in the brackish zone of the Westerschelde estuary. J Fish Biol 55:704–719CrossRefGoogle Scholar
  38. Hsü KJ, Montadert L, Bernoulli D, Cita MB, Erickson A, Garrison RE, Kidd RB, Mélières F, Müller C, Wright R (1977) History of the Mediterranean salinity crisis. Nature 267:399–403CrossRefGoogle Scholar
  39. Hudson RR, Coyne JA (2002) Mathematical consequences of the genealogical species concept. Evolution 56:1557–1565CrossRefGoogle Scholar
  40. Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383–2394CrossRefGoogle Scholar
  41. Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Syst 24:189–216CrossRefGoogle Scholar
  42. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  43. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B 265:2257–2263CrossRefGoogle Scholar
  44. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200CrossRefGoogle Scholar
  45. Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology and causes of the Messinian salinity crisis. Nature 400:652–655CrossRefGoogle Scholar
  46. Kuo C-H, Avise JC (2005) Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica 124:179–186CrossRefGoogle Scholar
  47. Lavoie DM, Smith LD, Ruiz GM (1999) The potential for intracoastal transfer of non-indigenous species in ballast water of ships. Estuar Coast Shelf Sci 48:551–564CrossRefGoogle Scholar
  48. Lawrie SM, Speirs DC, Raffaelli DG, Gurney WSC, Paterson DM, Ford R (1999) The swimming behaviour and distribution of Neomysis integer in relation to tidal flow. J Exp Mar Biol Ecol 242:95–106CrossRefGoogle Scholar
  49. Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate ‘populations’. Evolution 54:2014–2027CrossRefGoogle Scholar
  50. Maldonado A (1985) Evolution of the Mediterranean basins and a detailed reconstruction of the Cenozoic Paleoceanography. In: Margalef R (eds) Western Mediterranean. Pergamon Press, London, pp 17–56Google Scholar
  51. Maltagliati F (1999) Genetic divergence in natural populations of the Mediterranean killifish Aphanius fasciatus. Mar Ecol Prog Ser 179:155–162CrossRefGoogle Scholar
  52. Mauchline J (1980) The biology of mysids and euphausiids. In: Blaxter JHS, Russel FS, Yonge M (eds) Advances in marine biology (18). Academic, London, pp 681Google Scholar
  53. Mees J, Fockedey N, Hamerlynck O (1995) Comparative study of the hyperbenthos of three European estuaries. Hydrobiologia 311:153–174CrossRefGoogle Scholar
  54. Millot C (1999) Circulation in the Western Mediterranean Sea. J Mar Syst 20:423–442CrossRefGoogle Scholar
  55. Moffat AM, Jones MB (1993) Correlation of the distribution of Mesopodopsis slabberi (Crustacea, Mysidacea) with physico-chemical parameters in a partially-mixed estuary (Tamar, England). Neth J Aquat Ecol 27:155–162CrossRefGoogle Scholar
  56. Munilla T, San Vicente C (2005) Suprabenthic biodiversity of Catalan beaches (NW Mediterranean). Acta Oecol 27:81–91CrossRefGoogle Scholar
  57. Müller J (2000) Mitochondrial DNA variation and the evolutionary history of cryptic Gammarus fossarum types. Mol Phylogenet Evol 15:260–268CrossRefGoogle Scholar
  58. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  59. Nikula R, Vainola R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143:339–350CrossRefGoogle Scholar
  60. Nilsson T (1982) The Pleistocene: geology and life in the quaternary age. D. Ridel Publishing Co., DordrechtGoogle Scholar
  61. Palumbi S, Martin RA, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s Guide to PCR, Version 2. University of Hawaii Zoology Department, HonululuGoogle Scholar
  62. 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 128:73–82CrossRefGoogle Scholar
  63. Peijnenburg KTC, Breeuwer JAJ, Pierrot-Bults AC, Menken SBJ (2004) Phylogeography of the planktonic chaetogenath Sagitta setosa reveals isolation in European seas. Evolution 58:1472–1487CrossRefGoogle Scholar
  64. Perdices A, Carmona JA, Fernández-Delgado C, Doadrio I (2001) Nuclear and mitochondrial data reveal high genetic divergence among Atlantic and Mediterranean populations of the Iberian killifish Aphanius iberus (Teleostei: Cyprinodontidae). Heredity 87:314–324CrossRefGoogle Scholar
  65. Perez-Losada M, Guerra A, Sanjuan A (1999) Allozyme differentiation in the cuttlefish Sepia offcinalis (Mollusca: Cephalopoda) from the NE Atlantic and Mediterranean. Heredity 83:280–289CrossRefGoogle Scholar
  66. Pfenninger M, Staubach S, Albrecht C, Streit B, Schwenk K (2003) Ecological and morphological differentiation among cryptic evolutionary lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774). Mol Ecol 12:2731–2745CrossRefGoogle Scholar
  67. Pillai NK (1968) A revision of the genus Mesopodopsis Czerniavsky (Crustacea: Mysidacea). J Zool Soc India 20:6–24Google Scholar
  68. Por FD (1989) The legacy of the Tethys. An aquatic biogeography of the Levant. Kluwer, DordrechtCrossRefGoogle Scholar
  69. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  70. 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 12:521–524Google Scholar
  71. Remerie T, Bourgois T, Vanreusel A (2005) Morphological differentiation between geographically separated populations of Neomysis integer and Mesopodopsis slabberi (Crustacea, Mysida). Hydrobiologia 549:239–250CrossRefGoogle Scholar
  72. Roast SD, Widdows J, Jones MB (1998) The position maintenance behaviour of Neomysis integer (Peracarida: Mysidacea) in response to current velocity, substratum and salinity. J Exp Mar Biol Ecol 220:25–45CrossRefGoogle Scholar
  73. Rocha-Olivares A, Fleeger JW, Foltz DW (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod. Mol Biol Evol 18:1088–1102CrossRefGoogle Scholar
  74. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898CrossRefGoogle Scholar
  75. Rosenborg NA (2003) The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly and polyphyly in a coalescent model. Evolution 57:1465–1477CrossRefGoogle Scholar
  76. Sanjuan A, Comesaña AS, De Carlos A (1996) Macrogeographic differentiation by mtDNA restriction site analysis in the S.W. European Mytilus galloprovincialis Lmk. J Exp Mar Biol Ecol 198:89–100CrossRefGoogle Scholar
  77. Sardo AM, Morgado F, Soares AMVM (2005) Mesopodopsis slabberi (Crustacea: Mysidacea): can it be used in toxicity tests? Ecotox Environ Safe 60:81–86CrossRefGoogle Scholar
  78. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380CrossRefGoogle Scholar
  79. Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN. A software for population genetics data analysis, Version 2.00. University of Geneva, GenevaGoogle Scholar
  80. Schubart CD, Diesel R, Blair Hedges S (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365CrossRefGoogle Scholar
  81. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116CrossRefGoogle Scholar
  82. Solé M, Porte C, Barcelo D, Albaiges J (2000) Bivalves residue analysis for the assessment of coastal pollution in the Ebro Delta (NW Mediterranean). Mar Pollut Bull 40:746–753CrossRefGoogle Scholar
  83. 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 13:1377–1390CrossRefGoogle Scholar
  84. Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (* and other methods), Version 4.0. Sinauer Associates, SunderlandGoogle Scholar
  85. Tamura K, Nei M (1993) Estimations of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  86. Tattersall WM, Tattersall OS (1951) The British Mysidacea. Ray Society, London, p 460Google Scholar
  87. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  88. Tintore J, La Violette PE, Blade I, Cruzado A (1998) A study of an intense density front in the eastern Alboran Sea: the Almeria-Oran front. J Phys Oceanogr 18:1384–1397CrossRefGoogle Scholar
  89. Triantafyllidis A, Apostolidis AP, Katsares V, Kelly E, Mercer J, Hughes M, Jørstad KE, Tsolou A, Hynes R, Triantaphyllidis C (2005) Mitochondrial DNA variation in the European lobster (Homarus gammarus) throughout the range. Mar Biol 146:223–235CrossRefGoogle Scholar
  90. Wallis GP, Beardmore JA (1984) Genetic variation and environmental heterogeneity in some closely related goby species. Genetica 62:223–237CrossRefGoogle Scholar
  91. Watterson GA (1984) Lines of descent and the coalescent. Theor Popul Biol 26:77–93CrossRefGoogle Scholar
  92. Webb P, Wooldridge TH (1990) Diel horizontal migration of Mesopodopsis slabberi (Crustacea: Mysidacea) in Algoa Bay, southern Africa. Mar Ecol Prog Ser 62:73–78CrossRefGoogle Scholar
  93. Witt JDS, Blinn DW, Hebert PDN (2003) The recent evolutionary origin of the phenotypically novel amphipod Hyalella Montezuma offers an ecological explanation for morphological stasis in a closely allied species complex. Mol Ecol 12:405–413CrossRefGoogle Scholar
  94. Wittmann KJ (1992) Morphogeographic variations in the genus Mesopodopsis Czerniavsky with description of three new species (Crustacea, Mysidacea). Hydrobiologia 241:71–89CrossRefGoogle Scholar
  95. Wonham MJ, Carlton JT, Ruis GM, Smith LD (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Mar Biol 136:1111–1121CrossRefGoogle Scholar
  96. Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Cuzin-Roudy J, Buchholz F, Patarnello T (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica: Euphausiacea) from the North East Atlantic and the Mediterranean Sea. Mar Biol 136:191–199CrossRefGoogle Scholar
  97. 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 13:1785–1798CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Thomas Remerie
    • 1
    • 3
    Email author
  • Tine Bourgois
    • 1
  • Danny Peelaers
    • 1
  • Andy Vierstraete
    • 2
    • 3
  • Jacques Vanfleteren
    • 2
    • 3
  • Ann Vanreusel
    • 1
    • 3
  1. 1.Marine Biology Section, Biology DepartmentGhent UniversityGentBelgium
  2. 2.Biology DepartmentGhent UniversityGentBelgium
  3. 3.CeMoFE, Center for Molecular Phylogeny and EvolutionGhent UniversityGentBelgium

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