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.
Similar content being viewed by others
References
Choi SC (1977) Test of equality of dependent correlations. Biometrika 64:645–647
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
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
Johannesson K (2003) Evolution in Littorina: ecology matters. J Sea Res 49:107–117
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
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
Long JS (1997) Regression models for categorical and limited dependent variables. Sage, Thousand Oaks, CA
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
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
Reid DG, Dyal P, Williams ST (2012) A global molecular phylogeny of 147 periwinkle species (Gastropoda, Littorininae). Zoolog Scr 41:125–136
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
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
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
Warwick T, Knight AJ, Ward RD (1990) Hybridisation in the Littorina saxatilis species complex (Prosobranchia:Mollusca). Hydrobiologia 193:109–116
Wilding CS, Grahame JW, Mill PJ (2000a) Mitochondrial DNA CoI haplotype variation in sibling species of rough periwinkles. Heredity 85:62–74
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
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-013-9728-3