Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation

Abstract

Distinct ecotypes of the snail Littorina saxatilis, each linked to a specific shore microhabitat, form a mosaic-like pattern with narrow hybrid zones in between, over which gene flow is 10-30% of within-ecotype gene flow. Multi-locus comparisons cluster populations by geographic affinity independent of ecotype, while loci under selection group populations by ecotype. The repeated occurrence of partially reproductively isolated ecotypes and the conflicting patterns in neutral and selected genes can either be explained by separation in allopatry followed by secondary overlap and extensive introgression that homogenizes neutral differences evolved under allopatry, or by repeated evolution in parapatry, or in sympatry, with the same ecotypes appearing in each local site. Data from Spain, the UK and Sweden give stronger support for a non-allopatric model of ecotype formation than for an allopatric model. Several different non-allopatric mechanisms can, however, explain the repeated evolution of the ecotypes: (i) parallel evolution by new mutations in different populations; (ii) evolution from standing genetic variation; and (iii) evolution in concert with rapid spread of new positive mutations among populations inhabiting similar environments. These models make different predictions that can be tested using comprehensive phylogenetic information combined with candidate loci sequencing.

Figure 1.

Six ecotypes of Littorina saxatilis illustrating the extensive variation in shell size and form that is present within this species. All the individuals are adults of representative size and shape. Upper row from left to right: ‘neglecta’—an ecotype living in the empty shells of dead barnacles in the UK and France, ‘S’—a crab-resistant ecotype found on boulder shores along the Swedish west coast, ‘E’—a wave-resistant ecotype confined to granite cliffs on the Swedish west coast. Lower row from left to right: ‘groenlandica’—a large ecotype found in subarctic areas along with ecotypes of smaller size, ‘SU’—a wave-resistant Spanish ecotype and ‘RB’—a crab-resistant Spanish ecotype.

Figure 2.

The distribution of Littorina saxatilis S and E ecotypes and hybrid forms along a rocky shore of a Swedish island. This island is rather typical for the Swedish west coast in that its shore consists of a mosaic of boulders and cliffs, and the distribution of the two ecotypes strictly follows the microhabitat distribution with hybrid zones where the habitat shifts.

Figure 3.

Genetic clustering of contrasting ecotypes of Littorina saxatilis from Sweden, the UK and Spain based either (a,b) on multi-locus estimates of genetic distances (microsatellites and AFLP) or (c) inferred from the phylogeny of mtDNA. Ecotypes are denoted with letters according to the terminology used in the different countries where S, M and RB are crab-tolerant phenotypes and E, H and SU are wave-tolerant (see table 1 for details). Samples from the same geographical sites (sampled within 50–100 m distance) are encircled. Open circles, RB; closed circles, SU.