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Ecology and Evolution, 10 (3), pp. 1158–1179, 2020, ISSN: 2045-7758, (_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/ece3.5943).
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Janson K. 1983.
Selection and migration in two distinct phenotypes of Littorina saxatilis in Sweden.
The first experimental study assessing ecotype selection and migration in a Swedish site (“ANG”) using reciprocal transplantation. The experiment was replicated over four different seasons and generated information on selection and migration over a full year.
Erlandsson J, Johannesson K. 1994.
Sexual selection on female size in a marine snail, Littorina littorea (L).
J. Exp. Mar. Biol. Ecol. 181:145-157.
An early study that combined field data and lab experiments to assess assortative mating and sexual selection in Littorina. Results show that large females have higher mating success than small females.
Johannesson K, Johannesson B, Lundgren U. 1995.
Strong natural selection causes microscale allozyme variation in a marine snail.
Proc. Nat. Acad. Sci., USA 92:2602-2606.
A steep genetic cline from low to high shore in the gene for aspartate aminotransferase was followed through a period when a large algal-bloom killed all snails in the lower intertidal. The cline largely disappeared when low shore populations was restored by recruitment of snails from the high-shore. This was followed by a rapidly re-establishment of the steep cline over a couple of generations suggesting strong divergent selection.
Johannesson B. 1986.
Shell morphology of Littorina saxatilis Olivi: the relative importance of physical factors and predation.
Journal of Experimental Marine Biology and Ecology 102:183-195.
This experimental study showed wave ecotype of L. saxatilis being much more vulnerable to crab predation than crab ecotype, and that small snails are crushed, but large snails are pulled out of their shell through the aperture. This study demonstrates one of two main selection agents on shell phenotype in L. saxatilis, and see Le Pennec et al. 2017 below for the other.
Johannesson B, Johannesson K. 1996.
Population differences in behaviour and morphology in Littorina saxatilis: Phenotypic plasticity or genetic differentiation?
J. Zool. 240:475-493.
A common garden study that showed that phenotypic differences among three ecotypes of L. saxatilis is a result of both inherited differences and plasticity. Notably, also boldness was shown to have a substantial component of inheritance.
Johannesson K, Tatarenkov A. 1997.
Allozyme variation in a snail (Littorina saxatilis) – deconfounding the effects of microhabitat and gene flow.
This study used an orthogonal design to demonstrated that genetic differentiation in allozyme loci is an effect of both a restricted gene flow and divergent selection among ecotype populations (crab and wave) on small islands in a Swedish archipelago.
Rolán-Alvarez E, Erlandsson J, Johannesson K, Cruz R. 1999.
Mechanisms of incomplete prezygotic reproductive isolation in an intertidal snail; testing behavioural models in wild populations.
Journal of Evolutionary Biology 12:879–890.
Lab experiments and field observations showed strong assortative mating for both size and ecotype in Spanish L. saxatilis. Non-random distribution of ecotypes in the field and females rejecting males of assimilar ecotype were suggested using a modelling approach to explain these observations.
Sadedin, S., Hollander, J., Panova, M., Johannesson, K. & Gavrilets, S. 2009.
Case studies and mathematical models of ecological speciation. 3:Ecotype formation in a Swedish snail.
Molecular Ecology 18:4006–4023.
Mathematical models were parameterised with empirical data for migration and selection in ecotypes of L. saxatilis over a crab-wave contact zone showing that ecotype formation is rapid and smooth but speciation less straight forward. Indeed, some factors promoting ecotype formation instead might hamper speciation in this system.
Wilding CS, Butlin RK, Grahame J. 2001.
Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers.
Journal of Evolutionary Biology 14:611-619.
A now classical study introducing FST outlier analysis as a tool to pinpoint loci that diverge more than expected for neutral loci. The study used AFLP markers and found 5% of these being putatively under divergent selection or linked to selected loci, comparing crab and wave ecotypes in UK.
Cruz, R., Vilas, C., Mosquera, J. & García, C. 2004.
Relative contribution of dispersal and natural selection to the maintenance of a hybrid zone in Littorina.
Evolution 58, 2734–2746.
Reciprocal transplants of crab and wave ecotypes were done over vertical habitat shifts on Spanish shores. Observed effects of divergent selection and migration showed selection being important but migration less so to restore phenotype gradients, suggesting habitat preference being a secondary effect of divergence rather than a cause of it.
Johannesson K, Havenhand JN, Jonsson PR, Lindegarth M, Sundin A, Hollander J. 2008.
Male discrimination of female mucous trails permits assortative mating in a marine snail species.
This experimental study showed male snails being able to assess direction of trails and discriminate between crab and wave ecotype trails. This suggests one of several possible mechanisms resulting in assortative mating of ecotypes in contact zones.
Hollander J, Butlin RK. 2010.
The adaptive value of phenotypic plasticity in two ecotypes of a marine gastropod.
BMC Evolutionary Biology 10:333.
Earlier studies have shown shell shape traits to be partly plastic. This study showed the plasticity being adaptive when snails raised under different environmental conditions in the lab were released in different field environments. This suggests plasticity, as a trait, has been under natural selection in this case.
Johannesson K, Panova M, Kemppainen P, Rolán-Alvarez E, André C, Butlin RK, 2010.
Repeated evolution of reproductive isolation in a marine snail – unveiling mechanisms of speciation.
Philosophical Transactions of the Royal Society B (Biology) 365:1735-1747.
This combined review and opinion paper summarised the knowledge on parallel patterns of isolation between ecotypes of Littorina saxatilis and suggested alternative hypothesis of the evolution of these patterns, and how these could be tested using genomic data.
Reid DG, Dyal P, Williams ST. 2012.
A global molecular phylogeny of 147 periwinkle species (Gastropoda, Littorininae).
Zoologica Scripta 41:125-136.
A comprehensive 3-gene phylogeny covering 97% of all species of periwinkles (Littorininae) including species in the three large genera Littoraria, Echinolittorina and Littorina.
Butlin RK, Saura M, Charrier G, Jackson B, André C, Caballero A, Coyne JA, Galindo J, Grahame JW, Hollander J, Kemppainen P, Martínez-Fernández M, Panova M, Quesada H, Johannesson K, Rolán-Alvarez E. 2014.
Parallel evolution of local adaptation and reproductive isolation in the face of gene flow.
Using Bayesian analysis of genetic data, this study showed that reproductively isolated crab and wave ecotypes of L. saxatilis are formed by demographically parallel processes of divergence under gene flow.
Ravinet M, Westram A, Johannesson K, Butlin R, André C, Panova M. 2016.
Shared and non-shared genomic divergence in parallel ecotypes of Littorina saxatilis at a local scale.
Molecular Ecology 25:287-305.
Parallel phenotypic divergence might involve the same or different loci. This study showed that RAD outliers distinguishing local crab and wave ecotypes in three islands were only to a relatively low proportion shared among islands <10 km apart. Instead, roughly 80% of outliers were unique to each island.
Johannesson K and Butlin R. 2017.
What explains rare and conspicuous colours in a snail? – A test of time-series data against models of drift, migration or selection.
Manipulation that increased frequencies of naturally rare shell colours were followed over more than 20 generations in isolated (island) populations. Frequencies dropped after manipulation but leveled off under balancing selection. In addition, frequencies were affected by stochastic events and local variation in selection pressures.
Le Pennec G, Butlin RK, Jonsson PR, Larsson AI, Lindborg J, Bergström E, Westram AM, Johannesson K, 2017.
Adaptation to dislodgement risk on wave-swept rocky shores in the snail Littorina saxatilis.
PLoS ONE 12:e0186901.
Experimental tests in a high-speed flume showed that snails (L. saxatilis) from the wave end of a 75 m crab-wave habitat transect withstand roughly 3-4 times stronger water flows than snails from the crab end of the transect. Similar trends were demonstrated in lab reared snails (both newly hatched and adults. This suggested this trait being at least partly inherited and likely maintained under divergent selection.
Westram AM, Rafajlović M, Chaube P, Faria R, Larsson T, Panova M, Ravinet M, Blomberg A, Mehlig B, Johannesson K, Butlin R. 2018.
Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow.
Evolution Letters 2: 297-309.
Combining a hybrid zone analysis with a theoretical model of how neutral and non-neutral loci are expected to behave, this study identified a large number of non-neutral outliers over a wave-crab contact zone in L. saxatilis. Assisted by a draft reference genome, it was shown that a large majority of these outliers are located in distinct regions of three of 17 linkage groups (chromosomes).