Skip to main content

Advertisement

SpringerLink
Log in

Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae)

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The genetic relationships between morphologically indistinguishable marine and brackish-water populations of Monocelis lineata (O.F. Müller, 1774) (Proseriata: Monocelididae) were analysed by means of allozyme electrophoresis. Fifteen samples of M. lineata (13 from the Mediterranean and two from the Atlantic) from coastal marine and brackish-water habitats were examined for variation at 18 loci. Eleven loci were polymorphic in at least one population of M. lineata. Low levels of within-population genetic variability were found, with average observed and expected heterozygosity values ranging from H o=0.015±0.015 to 0.113±0.044, and from H e=0.028±0.028 to 0.138±0.054, respectively. The occurrence of a number of private alleles indicated a marked genetic divergence among populations of M. lineata, with Rogers’ genetic distances ranging from D R=0.003 to 0.676 and a highly significant F ST value (0.918±0.012, P<0.001). UPGMA (unweighted pair-group method using arithmetic average) cluster analysis and multidimensional scaling showed a clear genetic divergence between marine and brackish-water populations. Moreover, Atlantic and Mediterranean populations were sharply separated. Our results suggest that M. lineata is a complex of sibling species.

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. 3a, b

Similar content being viewed by others

References

  • Archie JW (1985) Statistical analysis of heterozygosity data: independent sample comparisons. Evolution 39:623–637

    Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

  • Ax P (1956) Les turbellariès des étangs côtiers du littoral méditerranéen de la France méridionale. Vie Milieu 5[Suppl]:1–215

    Google Scholar 

  • Battaglia B, Bisol PM, Fava G (1978) Genetic variability in relation to the environment in some marine invertebrates. In: Battaglia B, Beardmore J (eds) Marine organisms. Plenum, New York, pp 55–70

  • Benzie JAH, Williams ST (1998) Phylogenetic relationships among giant clam species (Mollusca: Tridacnidae) determined by protein electrophoresis. Mar Biol 132:123–133

    Article  CAS  Google Scholar 

  • Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952

    Article  Google Scholar 

  • Cannon LRG, Faubel A (1988) Turbellaria. In: Higgins RP, Thiele J (eds) Introduction to the study of meiofauna. Smithsonian, pp 273–282

  • Chao L, Carr DE (1993) The molecular clock and the relationship between population size and generation time. Evolution 47:688–690

    Google Scholar 

  • Cognetti G (1994) Colonization of brackish waters. Mar Pollut Bull 28:583–586

    Article  CAS  Google Scholar 

  • Cognetti G, Maltagliati F (2000) Biodiversity and adaptative mechanism in brackish water fauna. Mar Pollut Bull 40:7–14

    Article  CAS  Google Scholar 

  • Curini-Galletti M, Mura F (1998) Two new species of the genus Monocelis Ehrenberg, 1831 (Platyhelminthes Proseriata) from the Mediterranean, with a redescription of Monocelis lineata (O.F. Müller, 1774). Ital J Zool 65:207–217

    Google Scholar 

  • Curini-Galletti M, Puccinelli I (1998) The Gyratrix hermaphroditus species complex (Kalyptorhynchia: Polycystididae) in marine habitats of eastern Australia. Hydrobiologia 383:287–298

    Article  Google Scholar 

  • Curini-Galletti M, Puccinelli I, Martens PM (1989) Karyometrical analysis of ten species of the subfamily Monocelidinae (Proseriata, Platyhelminthes) with remarks on the karyological evolution of the Monocelididae. Genetica 78:169–178

    Google Scholar 

  • Danovaro R, Fraschetti S, Belgrano A, Vincx M, Curini-Galletti M, Albertelli G, Fabiano M (1995) The potential impact of meiofauna on the recruitment of macrobenthos in a subtidal coastal benthic community of the Ligurian sea (North-Western Mediterranean): a field result. In: Eleftheriou et al. (eds) Biology and ecology of shallow coastal waters. Olsen and Olsen, Denmark, pp 115–122

  • De Matthaeis E, Davolos D, Cobolli M, Ketmaier V (2000) Isolation by distance in equilibrium and nonequilibrium populations of four talitrid species in the Mediterranean sea. Evolution 54:1606–1613

    PubMed  Google Scholar 

  • Ekaratne K, Burfitt AH, Flowerdew MW, Crisp DJ (1982) Separation of the two Atlantic species of Pomatoceros, P. lamarkii and P. triqueter (Annelida: Serpulidae) by means of biochemical genetics. Mar Biol 71:257–264

    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 data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Fong PP, Garthwaite RL (1994) Allozyme electrophoresis analysis of the Hediste limnicola–H. diversicolor–H. japonica species complex (Polychaeta: Nereididae). Mar Biol 118:463–470

    CAS  Google Scholar 

  • Gillespie JH (1986) Variability of evolutionary rate of DNA. Genetics 113:1077–1091

    CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT version 1.2, a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guiller A, Bellido A, Madec L (1998) Genetic distances and ordination: the land snail Helix aspersa in North Africa as a test case. Syst Biol 47:208–227

    Article  CAS  PubMed  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372

    CAS  PubMed  Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802

    Google Scholar 

  • Hoffmann AA, Hercus MJ (2000) Environmental stress as an evolutionary force. Bioscience 50:217–225

    Google Scholar 

  • Hsu KJ, Ryan WBF, Cita MB (1973) Late Miocene desiccation of the Mediterranean. Nature 242:240–244

    CAS  Google Scholar 

  • Jondelius U, Ruiz-Trillo I, Baguñà J, Riutort M (2002) The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool Scr 31:201–215

    Article  Google Scholar 

  • Klautau M, Russo CAM, Lazoski C, Boury-Esnault N, Thorpe JP, Solé-Cava A (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Condrilla nucula. Evolution 53:1414–1422

    Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 132:295–303

    Google Scholar 

  • Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate ‘populations’. Evolution 54:2014–2027

    CAS  PubMed  Google Scholar 

  • Lucas JS, Nash WJ, Nishida M (1985) Aspects of the evolution of Acanthaster planci (L.) (Echinodermata: Asteroidea). In: Proceedings of the 5th International Coral Reef Symposium, Papeete, Tahiti, pp 327–332

  • Maltagliati F, Peru AP, Casu M, Rossi F, Lardicci C, Curini-Galletti M, Castelli A (2000) Is Syllis gracilis (Polychaeta: Syllidae) a species complex? An allozyme perspective. Mar Biol 136:871–879

    Article  CAS  Google Scholar 

  • Manchenko GP, Kulikova VI (1996) Allozyme and colour differences between two sibling species of the heteronemertean Lineus torquatus from Sea of Japan. Mar Biol 125:687–691

    Google Scholar 

  • Manchenko GP, Radashevsky VI (1998) Genetic evidence for two sibling species within Polydora cf. ciliata (Polychaeta: Spionidae) from the Sea of Japan. Mar Biol 131:489–495

    Article  CAS  Google Scholar 

  • Martens P (1984) Comparison of three different extraction methods for Turbellaria. Mar Ecol Prog Ser 14:229–234

    Google Scholar 

  • Martens PM, Schockaert ER (1986) The importance of turbellarians in the marine meiobenthos: a review. Hydrobiologia 132:295–303

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • Nevo E, Beiles A, Ben-Shlomo R (1984) The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: Mani GS (ed) Evolutionary dynamics of genetic diversity. Springer, Berlin Heidelberg New York, pp 13–213

  • Pasteur N, Pasteur G, Bonhomme F, Catalan F, Britton-Davidian J (1987) Manuel technique de génétique par électrophorèse des protéines. Lavoisier, Paris

  • Por FD (1989) The legacy of Tethys—an aquatic biogeography of the Levant. Monographiae Biologicae, vol 63. Kluwer, Dordrecht

  • Raymond M, Rousset F (1995) GENEPOP (ver 1.2): population genetic software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Riedl R (1983) Fauna und Flora des Mittelmeeres. Parey, Berlin

  • Rogers JS (1972) Measures of genetic similarity and genetic distance. Studies in Genetics, University of Texas Publication 7213, pp145–153

  • Ruiz-Trillo I, Riutort M, Littlewood DTJ, Herniou EA, Baguñà J (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of the Platyhelminthes. Science 283:1919–1923

    Article  CAS  PubMed  Google Scholar 

  • Sala E (2002) Marine biology in the 21st century: do we need to look at the past? Trends Ecol Evol 17:59–60

    Article  Google Scholar 

  • Sarà M (1985) Ecological factors and their biogeographic consequences in the Mediterranean ecosystems. In: Moraitou MM, Apostolopoulou MM, Kiortsis V (eds) Mediterranean marine ecosystems. Plenum, New York, pp 1–17

  • Sato M, Masuda Y (1997) Genetic differentiation in two sibling species of the brackish-water polychaete Hediste japonica complex (Nereididae). Mar Biol 130:163–170

    Article  CAS  Google Scholar 

  • Sbordoni V, Caccone A, Allegrucci G, Cesaroni D (1990) Molecular island biogeography. Atti Conv Lincei 85:55–83

    Google Scholar 

  • Scherer S (1990). The protein molecular clock. Evol Biol 24:83–106

    CAS  Google Scholar 

  • Selander R (1977) Genetic variation in natural populations. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland, pp 21–45

  • Shaklee JB, Allendorf FW, Morizot DC, Whitt GS (1990) Gene nomenclature for protein-coding loci in fish. Trans Am Fish Soc 119:2–15

    CAS  Google Scholar 

  • Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65

    Google Scholar 

  • Sopott-Ehlers (1993) Ultrastructural features of the pigmented eye spot in Pseudomonocelis agilis (Plathelminthes, Proseriata). Microfauna Marina 8:77–78

    Google Scholar 

  • StatSoft (1997) STATISTICA for Windows. Computer program manual. StatSoft, Tulsa, Okla., USA

  • Stocker TF (1992) A glimpse of the glacial. Nature 391:338–339

    Article  Google Scholar 

  • Swofford DL, Selander RB (1981) BIOSYS-1: a Fortran program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J Hered 72:282–283

    Google Scholar 

  • Thorpe JP (1982) The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Annu Rev Ecol Syst 13:139–168

    Article  CAS  Google Scholar 

  • Thorpe JP, Solé-Cava AM (1994) The use of allozyme electrophoresis in invertebrate systematics. Zool Scr 23:3–18

    Google Scholar 

  • Watzin C (1983) The effects of meiofauna on settling macrofauna: meiofauna may structure macrofaunal communities. Oecologia 59:163–166

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Gavino Oggiano for providing specimens of M. lineata from Keflavik, thanks to a grant allowed by the Sandgerđi Marine Centre, Iceland. Dr. Kennet Lundin (Göteborg) kindly provided the Swedish specimens of M. lineata. Dr. Anna Rita Correddu and Dr. Giovanni Vargiu assisted during electrophoretic analysis. Dr. Ferruccio Maltagliati gave a critical reading and helpful suggestions for the improvement of the manuscript. This research was partly supported by the European Community INTERREG III international project, and by the ‘Centro di eccellenza’ of the University of Sassari, Italy.

Author information

Authors and Affiliations

  1. Dipartimento di Zoologia e Antropologia Biologica, Via F. Muroni 25, 07100, Sassari, Italy

    Marco Casu & Marco Curini-Galletti

Authors
  1. Marco Casu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Curini-Galletti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Casu.

Additional information

Communicated by R. Cattaneo-Vietti, Genova

Appendix 1

Appendix 1

Table 5 gives allele frequencies at the 18 loci analysed.

Table 5 Allele frequencies at 18 allozyme loci. Private alleles are in bold. Numbers of individuals scored are given in parentheses
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casu, M., Curini-Galletti, M. Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae). Marine Biology 145, 669–679 (2004). https://doi.org/10.1007/s00227-004-1367-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-004-1367-x

Keywords

Search

Navigation