Skip to main content
Log in

Micro-spatial distribution of two sibling periwinkle species across the intertidal indicates hybrdization

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Populations of periwinkles Littorina saxatilis (Olivi 1792) and L. arcana Hannaford Ellis, 1978 are well suited for microevolutionary studies, being at the same time closely related and intraspecifically diverse. The divergence between these two sibling species, sympatric over large parts of their distribution areas, is small, the only morphological difference being the pallial gland complex structure in females. Molecular identification is possible with the use of a RAPD nuclear marker (cloned A2.8 DNA fragment) typical for L. arcana. However, in some individuals from sympatric populations molecular and morphological criteria suggest conflicting species affiliation, which may be explained either by hybridization or by shared ancestral polymorphism. We tested the hybridization hypotheses examining the micro-spatial distribution of these two species across the intertidal zone in two distant sites at the Barents Sea. We found that (a) the frequency of putative hybrids in sympatric populations was proportional to the frequency of L. arcana; (b) L. saxatilis bearing A2.8 DNA fragment were almost absent in the lower part of the intertidal zone, where L. arcana was absent too; (c) there was a close positive correlation between the distribution of potential parent molluscs and putative hybrids. Moreover, logistic regression models showed a good agreement between the distribution of putative hybrid frequencies and that of parental species frequencies. All our observations taken together support the hypothesis of hybridization between L. saxatilis and L. arcana. Elucidating the mechanisms that support the species status of these sympatric populations is necessary.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Choi SC (1977) Test of equality of dependent correlations. Biometrika 64:645–647

    Article  Google Scholar 

  • Doellman MM, Trussell GC, Grahame JW, Vollmer SV (2011) Phylogeographic analysis reveals a deep lineage split within North Atlantic Littorina saxatilis. Proc. R. Soc. B. 278:3175–3183

    Article  PubMed  Google Scholar 

  • Grahame JW, Wilding CS, Butlin RK (2006) Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis. Evolution 60:268–278

    PubMed  CAS  Google Scholar 

  • Johannesson K (2003) Evolution in Littorina: ecology matters. J Sea Res 49:107–117

    Article  Google Scholar 

  • Johannesson K, Panova M, Kemppainen P, Rolán-Alvarez E, Andre C, Butlin RK (2010) Repeated evolution of reproductive isolation in a marine snail—unveiling mechanisms of speciation. Phil. Trans. R. Soc. B 365:1735–1747

    Article  PubMed  Google Scholar 

  • Kemppainen P, Panova M, Hollander J, Johannesson K (2009) Complete lack of mitochondrial divergence between two species of NE Atlantic marine intertidal gastropods. J Evol Biol 22:2000–2011

    Article  PubMed  CAS  Google Scholar 

  • Long JS (1997) Regression models for categorical and limited dependent variables. Sage, Thousand Oaks, CA

    Google Scholar 

  • Mikhailova NA, Gracheva YA, Backeljau T, Granovitch AI (2009) A potential species-specific molecular marker suggests interspecific hybridization between sibling species Littorina arcana and L. saxatilis (Mollusca, Caenogastropoda) in natural populations. Genetica 137:333–340

    Article  PubMed  CAS  Google Scholar 

  • Myers JL, Well AD (2003) Research design and statistical analysis, 2nd ed. Lawrence Erlbaum, NJ

  • Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, London

    Google Scholar 

  • Reid DG, Dyal P, Williams ST (2012) A global molecular phylogeny of 147 periwinkle species (Gastropoda, Littorininae). Zoolog Scr 41:125–136

    Article  Google Scholar 

  • Rolán-Alvarez E (2007) Sympatric speciation as a by-product of ecological adaptation in the Galicia Littorina saxatilis hybrid zone. J Mollus Stud 73:1–10

    Article  Google Scholar 

  • Small MP, Gosling EM (2000) Genetic structure and relationships in the snail species complex Littorina arcana Hannaford Ellis, L. compressa Jeffreys and L. saxatilis (Olivi) in the British Isles using SSCPs of cytochrome-b fragments. Heredity 84:692–701

    Article  PubMed  CAS  Google Scholar 

  • Ward RD, Janson K (1985) A genetic analysis of sympatric subpopulations of the sibling species Littorina saxatilis Olivi and Littorina arcana Hannaford Ellis. J Mollus Stud 51:86–94

    Google Scholar 

  • Warwick T, Knight AJ, Ward RD (1990) Hybridisation in the Littorina saxatilis species complex (Prosobranchia:Mollusca). Hydrobiologia 193:109–116

    Article  Google Scholar 

  • Wilding CS, Grahame JW, Mill PJ (2000a) Mitochondrial DNA CoI haplotype variation in sibling species of rough periwinkles. Heredity 85:62–74

    Article  PubMed  CAS  Google Scholar 

  • Wilding CS, Grahame JW, Mill PJ (2000b) Nuclear DNA restriction site polymorphisms and the phylogeny and population structure of an intertidal snail species complex. Heredity 133:9–18

    CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the administration of the Murmansk Marine Biological Institute RAS and personally to Dr. Mikhail Makarov for providing logistic support for our field work and to Natalia Lentsman (Saint-Petersburg State University) for valuable advice on the improvement of the general logical structure and the English of the manuscript. This study was supported by a grant from the Russian Foundation for Basic Research (RFBR) no. 12-04-00312 and, partly, by SPbSU Project No. 1.0.140.2010.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Natalia A. Mikhailova.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Granovitch, A.I., Maximovich, A.N., Avanesyan, A.V. et al. Micro-spatial distribution of two sibling periwinkle species across the intertidal indicates hybrdization. Genetica 141, 293–301 (2013). https://doi.org/10.1007/s10709-013-9728-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-013-9728-3

Keywords

Navigation