Skip to main content
Log in

Electrophoretic heterogeneity within and between flat periwinkles (Mollusca: Gastropoda) along an intertidal transect at Ria Ferrol, northwest Spain

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Using isoelectric focusing of esterases (EST), general proteins (GP) and myoglobin (Mb), we surveyed intra- and interspecific differentiation in flat periwinkles along a vertical intertidal transect in the Ensenada do Baño at Ria Ferrol, N.W. Spain. In this region, L. obtusata occurs in four algal belts, although it is rare in the lowest zone defined by Fucus serratus. L. fabalis is common in the F. serratus and F. vesiculosus belt, but is absent higher up on Ascophyllum nodosum and F. spiralis. Our data show that (1) EST and GP consistently differentiate between L. obtusata and L. fabalis, without however providing useful diagnostic markers, (2) L. fabalis is the less variable (heterozygous), but more heterogeneous species, (3) Mb patterns show significant heterogeneity in L. obtusata between the F. serratus zone and the other algal belts, but not in L. fabalis, and (4) the data on littorinid Mb appear inconsistent with a dimeric protein controlled by a single locus. Yet, assuming two loci coding for a monomeric (or dissociated dimeric) protein produces for the flat periwinkles a data set in which no significant deviations from Hardy-Weinberg expectations were detected. Nevertheless, this speculative interpretation fails to explain all littorinid Mb data. Hence the genetics and structure of littorinid Mb need further study.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alyakrinskaya, I. O., 1989. Biochemical adaptations of some littoral molluscs to feeding. Zh. Evol. Biokhim. Fisiol. 25: 112–115. [in Russian].

    Google Scholar 

  • Alyakrinskaya, I. O., 1994. Haemoglobin concentration and its functional meaning in White Sea Littorina. Gidrobiol. Zh. 30: 69–78. [in Russian].

    Google Scholar 

  • Backeljau, T. & T. Warmoes, 1992. The phylogenetic relationships of ten Atlantic littorinids assessed by allozyme electrophoresis. In J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the Third International Symposium on Littorinid Biology. The Malacological Society of London, London: 9–24.

    Google Scholar 

  • Backeljau, T., K. Breugelmans, H. Leirs, T. Rodriguez, D. Sherbakov, T. Sitnikova, J.-M. Timmermans, J. L. Van Goethem & E. Verheyen, 1994. Application of isoelectric focusing in molluscan systematics. The Nautilus, Suppl. 2: 156–167.

    Google Scholar 

  • Berger, E. M., 1977. Gene-enzyme variation in three sympatric species of Littorina. II. The Roscoff populations, with a note on the origin of North American L. littorea. Biol. Bull. 153: 255–264.

    Google Scholar 

  • Berger, V. Y., A. N. Pakhomov & A. G. Mukhlenov, 1975. Study of isozyme composition of esterases and lactate dehydrogenase during adaptation of Littorina littorea (L.) (Gastropoda) to the changes in water salinity. Zh. Obsh. Biol. 36: 579–584. [in Russian].

    Google Scholar 

  • Bonaventura, J., C. Bonaventura & B. Sullivan, 1975. Hemoglobins and hemocyanins: comparative aspects of structure and function. J. exp. Zool. 194: 155–174.

    Google Scholar 

  • Buth, D. G., 1990. Genetic principles and the interpretation of electrophoretic data. In D. H. Whitmore (ed.), Electrophoretic and Isoelectric Focusing Techniques in Fisheries Management. CRC Press, Boca Raton: 1–21.

    Google Scholar 

  • Cavalli-Sforza, L. L. & A.W. F. Edwards, 1967. Phylogenetic analysis: models and estimation procedures. Evolution 21: 550–570.

    Google Scholar 

  • Dytham, C., J. Grahame & P. J. Mill, 1992. Esterase variation in Littorina arcana and L. saxatilis at Robin Hood's bay, Yorkshire. In J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the Third International Symposium on Littorinid Biology. The Malacological Society of London, London: 39–44.

    Google Scholar 

  • Gaffney, P. M., 1994. Heterosis and heterozygote deficiencies in marine bivalves: more light? In Beaumont, A. R. (ed.), Genetics and Evolution of Aquatic Organisms. Chapman & Hall, London: 146–153.

    Google Scholar 

  • Hilbish, T. J., 1985. Demographic and temporal structure of an allele frequency cline in the mussel Mytilus edulis. Mar. Biol. 86: 163– 171.

    Google Scholar 

  • Hilbish, T. J., 1996. Population genetics of marine species: interaction of natural selection and historically differentiated populations. J. exp. mar. Biol. Ecol. 200: 67–83.

    Google Scholar 

  • Janson, K., 1987a. Genetic drift in small and recently founded populations of the marine snail Littorina saxatilis. Heredity 58: 31–37.

    Google Scholar 

  • Janson, K., 1987b. Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. linn. Soc. 30: 245–256.

    Google Scholar 

  • Janson, K. & R. D. Ward, 1984. Microgeographic variation in allozyme and shell characters in Littorina saxatilis Olivi (Prosobranchia: Littorinidae). Biol. J. linn. Soc. 22: 289–307.

    Google Scholar 

  • Johannesson, K., 1992. Genetic variability and large scale differentiation in two species of littorinid gastropods with planktotrophic development, Littorina littorea (L.) and Melarhaphe (Littorina) neritoides (L.) (Prosobranchia: Littorinacea), with notes on a mass occurrence of M. neritoides in Sweden. Biol. J. linn. Soc. 47: 285–299.

    Google Scholar 

  • Johannesson, K. & B. Johannesson, 1989. Differences in allele frequencies of Aat between high-and mid-rocky shore populations of Littorina saxatilis (Olivi) suggest selection at this enzyme locus. Genet. Res. Cambridge 54: 7–11.

    Google Scholar 

  • Johannesson, K., B. Johannesson & E. Rolán-Alvarez, 1993. Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marine snail Littorina saxatilis. Evolution 47: 1770–1787.

    Google Scholar 

  • Johannesson, K., E. Rolán-Alvarez & A. Ekendahl, 1995a. Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution 49: 1180–1190.

    Google Scholar 

  • Johannesson, K., B. Johannesson & U. Lundgren, 1995b. Strong natural selection causes microscale allozyme variation in a marine snail. Proc. Natl. Acad. Sci. U.S.A. 92: 2602–2606.

    Google Scholar 

  • Johnson, M. S. & R. Black, 1982. Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar. Biol. 70: 157–164.

    Google Scholar 

  • Johnson, M. S. & R. Black, 1984. Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38: 1371–1383.

    Google Scholar 

  • Koehn, R. K., A. J. Zera & J. G. Hall, 1983. Enzyme polymorphism and natural selection. In M. Nei & R. K. Koehn (eds), Evolution of Genes and Proteins. Sinauer, Sunderland, Massachusetts: 115–136.

    Google Scholar 

  • Mangum, C. P., 1996. Subunit composition of polymorphic hemocyanins in the decapod crustaceans: differences between sibling species. Physiol. Zool. 69: 568–585.

    Google Scholar 

  • Mangum, C. P. & J. Greaves, 1996. Hemocyanins of the genus Uca: structural polymorphisms and native oligomers. J. exp. mar. Biol. Ecol. 199: 1–15.

    Google Scholar 

  • Mangum, C. P. & A. L. McKenney, 1996. Subunit composition of the crustacean hemocyanins: divergence in incipient speciation. Biol. Bull. 191: 33–41.

    Google Scholar 

  • Medeiros, R., L. Serpa, C. Brito, H. De Wolf, K. Jordaens, B. Winnepenninckx & T. Backeljau, 1998. Radular myoglobin and protein variation within and among some littorinid species (Mollusca: Gastropoda). Hydrobiologia 378: 43–51.

    Google Scholar 

  • Mill, P. J. & J. Grahame, 1988. Esterase variability in the gastropods Littorina saxatilis (Olivi) and L. arcana Ellis. J. moll. Stud. 54: 347–353.

    Google Scholar 

  • Mill, P. J. & J. Grahame, 1992. Clinal changes in esterase variability in Littorina saxatilis (Olivi) and L. arcana Hannaford Ellis in southern Britain. In J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the Third International Symposium on Littorinid Biology. The Malacological Societyof London, London: 31–38.

    Google Scholar 

  • Newkirk, G. F. & R. W. Doyle, 1979. Clinal variation at an esterase locus in Littorina saxatilis and L. obtusata. Can. J. Genet. Cytol. 21: 505–513.

    Google Scholar 

  • Oxford, G. S., 1975. Food induced esterase phenocopies in the snail Cepaea nemoralis. Heredity 35: 361–370.

    Google Scholar 

  • Oxford, G. S., 1978. The nature and distribution of food-induced esterases in helicid snails. Malacologia 17: 331–339.

    Google Scholar 

  • Read, K. R. H., 1968. The myoglobins of the gastropod molluscs Busycon contrarium Conrad, Lunatia heros Say, Littorina littorea L. and Siphonaria gigas Sowerby. Comp. Biochem. Physiol. 25: 81–94.

    Google Scholar 

  • Reid, D. G., 1990. Note on the discrimination of females of Littorina mariae Sacchi & Rastelli and L. obtusata (Linnaeus). J. moll. Stud. 56: 113–114.

    Google Scholar 

  • Reid, D. G., 1996. Systematics and evolution of Littorina. The Ray Society, London, 463 pp.

    Google Scholar 

  • Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Google Scholar 

  • Rohlf, F. J., 1993. NTSYS-pc: numerical taxonomy and multivariate analysis system, version 1.80. Applied Biostatistics Inc., Setauket, New York.

    Google Scholar 

  • Rolán-Alvarez, E., C. Zapata & G. Alvarez, 1995. Distinct genetic subdivision in sympatric and sibling species of the genus Littorina (Gastropoda: Littorinidae). Heredity 74: 1–9.

    Google Scholar 

  • Sacchi, C. F. & M. Rastelli, 1966. Littorina mariae, nov. sp.: les differences morphologiques et écologiques entre ‘nains’ et ‘normaux’ chez l’‘espèce’ L. obtusata (L.) (Gastr. Prosobr.) et leur signification adaptive et évolutive. Atti Soc. Ital. Sci. Nat. Mus. Civ. Stor. Nat. Milano 105: 351–369.

    Google Scholar 

  • Swofford, D. L. & R. K. Selander, 1981. BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J. Hered. 72: 281–283.

    Google Scholar 

  • Tatarenkov, A. N., 1995a. Genetic divergence between sibling species Littorina mariae Sacchi & Rastelli and L. obtusata (L.) (Mollusca: Gastropoda) from the White Sea. Ophelia 40: 207–218.

    Google Scholar 

  • Tatarenkov, A. N., 1995b. Genetic heterogeneity in populations of Littorina brevicula (Philippi) (Mollusca: Gastropoda) in the northern part of Peter the Great Bay (Sea of Japan). Veliger 38: 85–91.

    Google Scholar 

  • Tatarenkov, A. & K. Johannesson, 1994. Habitat related allozyme variation on a microgeographic scale in the marine snail Littorina mariae (Prosobranchia: Littorinacea). Biol. J. linn. Soc. 53: 105– 125.

    Google Scholar 

  • Terwilliger, R. C. & R. H. Read, 1969. The radular muscle myoglobins of the amphineuran mollusc, Acanthopleura granulata Gmelin. Comp. Biochem. Physiol. 29: 551–560.

    Google Scholar 

  • Vuilleumier, F. & M. B. Matteo, 1972. Esterase polymorphisms in European and American populations of the periwinkle Littorina littorea (Gastropoda). Experientia 28: 1241–1242.

    Google Scholar 

  • Ward, R. D., 1990. Biochemical genetic variation in the genus Littorina (Prosobranchia: Mollusca). Hydrobiologia 193: 53–69.

    Google Scholar 

  • Warmoes, T., T. Backeljau & L. De Bruyn, 1988. The littorinid fauna of the Belgian coast (Mollusca, Gastropoda). Bull. Inst. r. Sci. nat. Belg. 58: 51–70.

    Google Scholar 

  • Wium-Andersen, G., 1970. Haemoglobin and protein variation in three species of Littorina. Ophelia 8: 267–273.

    Google Scholar 

  • Zaslavskaya, N. I., S. O. Sergievsky & A. N. Tatarenkov, 1992. Allozyme similarity of Atlantic and Pacific species of Littorina (Gastropoda: Littorinidae). J. moll. Stud. 58: 377–384.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olabarria, C., Timmermans, JM. & Backeljau, T. Electrophoretic heterogeneity within and between flat periwinkles (Mollusca: Gastropoda) along an intertidal transect at Ria Ferrol, northwest Spain. Hydrobiologia 378, 11–19 (1998). https://doi.org/10.1023/A:1003252500038

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003252500038

Navigation