Skip to main content

Advertisement

SpringerLink
Log in

Atlantic-Mediterranean and within-Mediterranean molecular variation in Coris julis (L. 1758) (Teleostei, Labridae)

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

Abstract

Sequence variation in the mitochondrial control region was studied in the Mediterranean rainbow wrasse (Coris julis), a species with pronounced pelagic larval phase inhabiting the Mediterranean Sea and the adjacent coastal eastern Atlantic Ocean. A total of 309 specimens from 19 sampling sites were analysed with the aim of elucidating patterns of molecular variation between the Atlantic and the Mediterranean as well as within the Mediterranean Sea. Phylogeographic analyses revealed a pronounced structuring into a Mediterranean and an Atlantic group. Samples from a site at the Moroccan Mediterranean coast in the Alboran Sea showed intermediate frequencies of “Mediterranean” and “Atlantic” haplotypes. We recognised a departure from molecular neutrality and a star-like genealogy for samples from the Mediterranean Sea, which we propose to have happened due to a recent demographic expansion. The results are discussed in the light of previous studies on molecular variation in fish species between the Atlantic and the Mediterranean and within the Mediterranean.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:16–723

    Google Scholar 

  • Arnaud-Haond S, Migliaccio M, Diaz-Almela E, Teixeira S, van de Vliet MS, Alberto F, Procaccini G, Duarte CM, Serrao EA (2007) Vicariance patterns in the Mediterranean Sea: east–west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J Biogeogr 34:963–976

    Article  Google Scholar 

  • Aurelle D, Guillemaud T, Afonso P, Morato T, Wirtz P, Santos RS, Cancela ML (2003) Genetic study of Coris julis (Osteichtyes, Perciformes, Labridae) evolutionary history and dispersal abilities. CR Biol 326:771–785

    Article  CAS  Google Scholar 

  • Bacci G, Razzauti A (1957) Falso gonocorismo in Coris julis (L.). Rend Acc Lincei Serie 8 23(3–4):181–189

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 Evolution Biol 16:1149–1158

    Article  CAS  Google Scholar 

  • Bentivegna F, Cirino P (1984) Sexual inversion in Coris julis L. 1758. Cybium 8(2):51–61

    Google Scholar 

  • Bergek S, Bjorklund M (2009) Genetic and morphological divergence reveals local subdivision of perch (Perca fluviatilis L.). Biol J Linn Soc 96:746–758

    Article  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  CAS  PubMed  Google Scholar 

  • Burford MO (2009) Demographic history, geographical distribution and reproductive isolation of distinct lineages of blue rockfish (Sebastes mystinus), a marine fish with a high dispersal potential. J Evol Biol 22(7):1471–1486

    Article  PubMed  Google Scholar 

  • Carlsson J, McDowell JR, Diaz-Jaimes P, Carlsson JEL, Boles SB, Gold JR, Graves JE (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 13:3345–3356

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Debes PV, Zachos FE, Hanel R (2008) Mitochondrial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic. Mol Ecol 17:3873–3888

    Article  CAS  PubMed  Google Scholar 

  • Domingues VS, Alexandrou M, Almada VC, Robertson DR, Brito A, Santos RS, Bernardi G (2008) Tropical fishes in a temperate sea: evolution of the wrasse Thalassoma pavo and the parrotfish Sparisoma cretense in the Mediterranean and the adjacent Macaronesian and Cape Verde Archipelagos. Mar Biol 154:465–474

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fitzpatrick BM (2009) Power and sample size for nested analysis of molecular variance. Mol Ecol 18(19):3961–3966

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galtier N, Nabholz B, Glémin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18(22):4541–4550

    Article  CAS  PubMed  Google Scholar 

  • Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. PNAS 104:858–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordoa A, Molì B, Raventos N (2000) Growth performance of four wrasse species on the north-western Mediterranean coast. Fish Res 45:43–50

    Article  Google Scholar 

  • Guillemaud T, Cancela ML, Afonso P, Morato T, Santos RS, Wirtz P (2000) Molecular insights into the taxonomic status of Coris atlantica (Pisces:Labridae). J Mar Biol Ass UK 80:929–933

    Article  CAS  Google Scholar 

  • Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18(23):4734–4756

    Article  PubMed  Google Scholar 

  • Gysels ES, Hellemans B, Patarnello T, Volckaert FAM (2004) Current and historic gene flow of the sand goby Pomatoschistus minutus on the European Continental Shelf and in the Mediterranean Sea. Biol J Lin Soc 83:561–576

    Article  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 H, Rogers A (2000) Genetic perspectives on human origins and differentiation. Annu Rev Genomics Hum Genet 1:361–385

    Article  CAS  PubMed  Google Scholar 

  • Hefti-Gautschi B, Pfunder M, Jenni L, Keller V, Ellegren H (2009) Identification of conservation units in the European Mergus merganser based on nuclear and mitochondrial DNA markers. Conserv Genet 10:87–99

    Article  CAS  Google Scholar 

  • Hoarau G, Piquet AM-T, van der Veer HW, Rijnsdorp AD, Stama WT, Olsena JL (2003) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190

    Article  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267

    Article  CAS  PubMed  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. PNAS 86:6196–6200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruskal JB (1964a) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27

    Article  Google Scholar 

  • Kruskal JB (1964b) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:28–42

    Google Scholar 

  • Larsson LC, Laikre L, Palm S, André C, Carvalho GR, Ryman N (2007) Concordance of allozyme and microsatellite differentiation in a marine fish, but evidence of selection at a microsatellite locus. Mol Ecol 16(6):1135–1147

    Article  CAS  PubMed  Google Scholar 

  • Laurent L, Lejeune P (1988) Coexistence en Méditerranée de deux livrées terminales différentes chez la girelle Coris julis (Pisces, Labridae). Cybium 12(1):91–95

    Google Scholar 

  • Lejeune P (1982) A propos de quelques Poissons de la Mediterraneé. Rev Francaise d’Aquariologie 9(1):27–32

    Google Scholar 

  • Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evolution Biol 18:70–80

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lipej L, Mavric B, Orlando Bonaca M (2009) Recent changes in the adriatic fish fauna–experiences from Slovenia. Varstvo Narave 22:91–96

    Google Scholar 

  • Maggio T, Lo Brutto S, Garoia F, Tinti F, Arculeo M (2009) Microsatellite analysis of red mullet Mullus barbatus (Perciformes, Mullidae) reveals the isolation of the Adriatic Basin in the Mediterranean Sea. ICES J Mar Sci 66:1883–1891

    Article  Google Scholar 

  • Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum Biol 76(2):173–190

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mejri R, Arculeo M, Ben Hassine OK, Lo Brutto S (2011) Genetic architecture of the marbled goby Pomatoschistus marmoratus (Perciformes, Gobiidae) in the Mediterranean Sea. Mol Phyl Evol 58(2):395–403

    Article  PubMed  Google Scholar 

  • Miller MP (2005) Alleles in space: computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724

    Article  CAS  PubMed  Google Scholar 

  • Monmonier M (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 3:245–261

    Google Scholar 

  • Nielsen EE, Hansen M, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol Ecol 15(11):3219–3229

    Article  CAS  PubMed  Google Scholar 

  • Nikula R, Väinölä R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143(2):339–350

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13(1):S146–S158

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Piron M, Balasso E, Poloniato D, Odorico R (2007) First record of Coris julis in the Miramare natural marine reserve. Ann Ser Hist Nat 17(2):165–170

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Poulain P-M (2001) Adriatic Sea surface circulation as derived from drifter data between 1990 and 1999. J Mar Syst 29:3–32

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Raventòs N, Macpherson E (2001) Planktonic larval duration and settlement marks on the otoliths of Mediterranean littoral fishes. Mar Biol 138:1115–1120

    Article  Google Scholar 

  • Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

    Article  CAS  PubMed  Google Scholar 

  • Roede MJ (1966) Notes on the labrid fish Coris julis (Linnaeus, 1758) with emphasis on dichromatism and sex. Vie Milieu 17(3):1317–1333

    Google Scholar 

  • Rohlf FJ (2007) NTSYSpc: numerical taxonomy system, ver. 2.20. Exeter Publishing Ltd, Setauket, NY

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Sa-Pinto A, Baird SJE, Pinho C, Alexandrino P, Branco M (2010) A three-way contact zone between forms of Patella rustica (Mollusca: Patellidae) in the central Mediterranean Sea. Biol J Linn Soc 100(1):154–169

    Article  Google Scholar 

  • Serra IA, Innocenti AM, Di Maida G, Calvo S, Migliaccio M, Zambianchi E, Pizzigalli C, Arnaud-Haond S, Duarte CM, Serrao EA, Procaccini G (2010) Genetic structure in the Mediterranean seagrass Posidonia oceanica: disentangling past vicariance events from contemporary patterns of gene flow. Mol Ecol 19:557–568

    Article  CAS  PubMed  Google Scholar 

  • Shaw PW, Turan C, Wright CM, O’Connel M, Carvalo GR (1999) Microsatellite DNA analysis of population structure in Atlantic herring (Clupea harengus), with direct comparison to allozyme and mtDNA RFLP analyses. Heredity 83:490–499

    Article  CAS  PubMed  Google Scholar 

  • Slade RW, Moritz C, Heideman A (1994) Multiple nuclear-gene phylogenies: applications to pinnipeds and comparison with a mitochondrial DNA gene phylogeny. Mol Biol Evol 11:341–356

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stepien CA, Rosenblatt RH, Bargmeyer BA (2001) Phylogeography of the spotted sand bass, Paralabrax maculatofasciatus: divergence of Gulf of California and Pacific Coast populations. Evolution 55(9):1852–1862

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

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

    Article  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  PubMed  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the kind contribution of Enrico Arneri, Ferdinando Boero, G. Andrea de Lucia, Paolo Domenici, Maria Ghelia, Menachem Goren, Paolo Guidetti, Miquel Palmer, Sergio Ragonese, Alfonso Toscano and Nedo Vrgoc who helped in obtaining specimens for analysis.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia “M. La Greca”, University of Catania, via Androne 81, 95124, Catania, Italy

    Carmelo Fruciano, Concetta Tigano & Venera Ferrito

  2. Institute of Fisheries Ecology, Johann Heinrich von Thünen-Institut (vTI), Federal Research Institute for Rural Areas, Forestry and Fisheries, Palmaille 9, 22767, Hamburg, Germany

    Reinhold Hanel

  3. Department of Biology, Dalhousie University, 1355 Oxford Street, B3H 4J, Halifax, Canada

    Paul V. Debes

Authors
  1. Carmelo Fruciano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reinhold Hanel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul V. Debes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Concetta Tigano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Venera Ferrito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carmelo Fruciano.

Additional information

Communicated by M. I. Taylor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fruciano, C., Hanel, R., Debes, P.V. et al. Atlantic-Mediterranean and within-Mediterranean molecular variation in Coris julis (L. 1758) (Teleostei, Labridae). Mar Biol 158, 1271–1286 (2011). https://doi.org/10.1007/s00227-011-1647-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1647-1

Keywords

Search

Navigation