Kerstin Johannesson

The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)?

In benthic invertebrates dispersal of planktotrophic larvae is generally considered more effective than is, for example, the rafting of adults or egg masses. It is certainly true that over short distances, viz., in the range of tens of kilometres or less, a moderately long-lived planktotrophic larva represents an effective mechanism of dispersal. However, turbulent mixing and mortality will decrease the concentration of planktotrophic larvae, and at some distance from the ancestral population the density of settlers may be too low to enable future matings between adults of low mobility. On the other hand, adults, juveniles or benthic egg masses drifted over long distances may colonize new habitats. The crucial point is the type of larval development of the organism. If the founder group belongs to a species with direct development or which produces very short-lived planktonic larvae, the low mobility of all life-stages will maintain a population within a restricted area so that mates will be likely to encounter each other even in a small population. Even if transport of benthic stages happens very rarely, this may be more influential than larval dispersal over long distances. To show that this may be true the detailed geographical distribution of two intertidal gastropod species with contrasting modes of development is presented and further support from the literature for this hypothesis is discussed.

Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea.

Marginal populations are often isolated and under extreme selection pressures resulting in anomalous genetics. Consequently, ecosystems that are geographically and ecologically marginal might have a large share of genetically atypical populations, in need of particular concern in management of these ecosystems. To test this prediction, we analysed genetic data from 29 species inhabiting the low saline Baltic Sea, a geographically and ecologically marginal ecosystem. On average Baltic populations had lost genetic diversity compared to Atlantic populations: a pattern unrelated to dispersal capacity, generation time of species and taxonomic group of organism, but strongly related to type of genetic marker (mitochondrial DNA loci had lost c. 50% diversity, and nuclear loci 10%). Analyses of genetic isolation by geographic distance revealed clinal patterns of differentiation between Baltic and Atlantic regions. For a majority of species, clines were sigmoid with a sharp slope around the Baltic Sea entrance, indicating impeded gene flows between Baltic and Atlantic populations. Some species showed signs of allele frequencies being perturbed at the edge of their distribution inside the Baltic Sea. Despite the short geological history of the Baltic Sea (8000 years), populations inhabiting the Baltic have evolved substantially different from Atlantic populations, probably as a consequence of isolation and bottlenecks, as well as selection on adaptive traits. In addition, the Baltic Sea also acts a refuge for unique evolutionary lineages. This marginal ecosystem is thus vulnerable but also exceedingly valuable, housing unique genes, genotypes and populations that constitute an important genetic resource for management and conservation.

INVITED REVIEW: Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea

Marginal populations are often isolated and under extreme selection pressures resulting in anomalous genetics. Consequently, ecosystems that are geographically and ecologically marginal might have a large share of genetically atypical populations, in need of particular concern in management of these ecosystems. To test this prediction, we analysed genetic data from 29 species inhabiting the low saline Baltic Sea, a geographically and ecologically marginal ecosystem. On average Baltic populations had lost genetic diversity compared to Atlantic populations: a pattern unrelated to dispersal capacity, generation time of species and taxonomic group of organism, but strongly related to type of genetic marker (mitochondrial DNA loci had lost c. 50% diversity, and nuclear loci 10%). Analyses of genetic isolation by geographic distance revealed clinal patterns of differentiation between Baltic and Atlantic regions. For a majority of species, clines were sigmoid with a sharp slope around the Baltic Sea entrance, indicating impeded gene flows between Baltic and Atlantic populations. Some species showed signs of allele frequencies being perturbed at the edge of their distribution inside the Baltic Sea. Despite the short geological history of the Baltic Sea (8000 years), populations inhabiting the Baltic have evolved substantially different from Atlantic populations, probably as a consequence of isolation and bottlenecks, as well as selection on adaptive traits. In addition, the Baltic Sea also acts a refuge for unique evolutionary lineages. This marginal ecosystem is thus vulnerable but also exceedingly valuable, housing unique genes, genotypes and populations that constitute an important genetic resource for management and conservation.

MORPHOLOGICAL DIFFERENTIATION AND GENETIC COHESIVENESS OVER A MICROENVIRONMENTAL GRADIENT IN THE MARINE SNAIL LITTORINA SAXATILIS

The marine gastropod Littorina saxatilis has different ecotypes in shores only a few meters apart. This has both taxonomic and evolutionary implications. Here we report on an extreme type of within‐shore dimorphism in shell characters. In the wave‐exposed rocky shores in northwestern Spain, we found one form of L. saxatilis in the upper‐level barnacle zone. It had a white, ridged shell, with black bands in the grooves. Another form confined to the lower‐shore mussel belt had a smooth shell that was either white and tessellated or darkly colored. These two forms cooccured in a narrow midshore zone together with individuals that had combined characters, but were present in low frequencies (11%–29%). We used principal‐component analysis of metric shell characters to study variation in shell size and shape. We found that the upper‐shore form was larger than the lower‐shore form. We also found small but significant differences in shell shape. Experiments in a common laboratory environment suggested the differences in shell ornamentation and color are inherited, but the individuals did not develop the morph‐specific characters until a shell height of about 3 mm. The occurrence of mainly two distinct forms may suggest the presence of two species that hybridize. An analysis of five polymorphic enzyme loci in populations of snails from three geographically separated sites indicated, however, that there was no positive correlation between morphological distances and genetic distances among populations on a geographic scale (tens of kilometers). Thus, we rejected the hypothesis of two species. However, on a microgeographic scale (meters), genetic differentiation between groups with the same form was less than differentiation between forms. This indicated a partial barrier to gene flow between the two forms, and preliminary mate choice data suggested this was caused by nonrandom mating in the midshore zone of overlap.

INCIPIENT REPRODUCTIVE ISOLATION BETWEEN TWO SYMPATRIC MORPHS OF THE INTERTIDAL SNAIL LITTORINA SAXATILIS

The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub‐groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone.

The maintenance of a cline in the marine snail Littorina saxatilis: The role of home site advantage and hybrid fitness

Steep clinal transitions in one or several inherited characters between genetically distinct populations are usually referred to as hybrid zones. Essentially two different mechanisms may maintain steep genetic clines. Either selection acts against hybrids that are unfit over the entire zone due to their mixed genetic origin (endogenous selection), or hybrids and parental types attain different fitness values in different parts of the cline (exogenous selection). Survival rate estimates of hybrids and parental forms in different regions of the cline may be used to distinguish between these models to assess how the cline is maintained. We used reciprocal transplants to test the relative survival rates of two parental ecotypes and their hybrids over microscale hybrid zones in the direct‐developing marine snail Littorina saxatilis (Olivi) on the rocky shores of Galicia, Spain. One of the parental forms occupies upper and the other lower shores, and the hybrids are found at various proportions (1–38%) along with both parental forms in a midshore zone a few meters wide. The survival rate over one month was 39‐52% of the native ecotype on upper shores, but only 2‐8% for the lower‐shore ecotype. In contrast, only 4‐8% of the upper‐shore ecotype but 53% of large (> 6 mm) and 8% of small (3‐6 mm) native lower‐shore ecotype survived in the lower shores. In the midshores, both the two parental ecotypes and the hybrids survived about equally well. Thus there is a considerable advantage for the native ecotypes in the upper and lower shores, while in the hybrid zone none of the morphs, hybrids included, are favored. This indicates that the dimorphism of L. saxatilis is maintained by steep cross‐shore selection gradients, thus supporting the selection‐gradient model of hybrid zones. We performed field and laboratory experiments that suggest physical factors and predation as important selective agents. Earlier studies indicate assortative mating between the two ecotypes in the midshore. This is unexpected in a hybrid zone maintained by selection gradients, and it seems as if the reproductive barrier compresses the hybrid zone considerably.

Parallel speciation: a key to sympatric divergence

Until recently, our view of speciation was that reproductive isolation evolves during long periods of allopatry through the accumulation of genetic differences that result in genetic incompatibility. This view now contrasts with new findings that characters affecting reproductive isolation can diverge rapidly in sympatry as a result of natural selection. Recent studies combining research on phylogeny and ecology of natural populations cast new light on patterns, timescales and mechanisms, and emphasize the role of ecological factors in speciation. Studies of parallel speciation provide a strong case for sympatric speciation and for natural selection generating reproductive barriers.

Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes.

Theory suggests that speciation is possible without physical isolation of populations (hereafter, nonallopatric speciation), but recent nonallopatric models need the support of irrefutable empirical examples. We collected snails (Littorina saxatilis) from three areas on the NW coast of Spain to investigate the population genetic structure of two ecotypes. Earlier studies suggest that these ecotypes may represent incipient species: a large, thick‐shelled ‘RB’ ecotype living among the barnacles in the upper intertidal zone and a small, thin‐shelled ‘SU’ ecotype living among the mussels in the lower intertidal zone only 10–30 m away. The two ecotypes overlap and hybridize in a midshore zone only 1–3 m wide. Three different types of molecular markers [allozymes, mitochondrial DNA (mtDNA) and microsatellites] consistently indicated partial reproductive isolation between the RB and the SU ecotypes at a particular site. However, each ecotype was related more closely to the other ecotype from the same site than to the same ecotype from another site further along the Galician coast (25–77 km away). These findings supported earlier results based solely on allozyme variation and we could now reject the possibility that selection produced these patterns. The patterns of genetic variation supported a nonallopatric model in which the ecotypes are formed independently at each site by parallel evolution and where the reproductive barriers are a byproduct of divergent selection for body size. We argue that neither our laboratory hybridization experiments nor our molecular data are compatible with a model based on allopatric ecotype formation, secondary overlap and introgression.

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

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.

Evolution in Littorina: ecology matters

Organisms of marine rocky shores are exposed to physical stress from abiotic factors, such as temperature, salinity and wave action. These factors vary over compressed temporal and spatial scales, producing an exceedingly heterogeneous habitat with steep gradients of selection, and it seems likely that this has a strong influence on the evolution of populations of rocky shore organisms. With the periwinkles (genus Littorina) as a model group, I review strategies for coping with small-scale heterogeneous environments and what implications these strategies have on the evolution of these species. Some species of Littorina have long-lived pelagic larvae and sites of various habitats are thus recruited from a common gene pool. This largely prevents local adaptation but minor adjustments are possible through a plastic phenotype. Other species of the genus are directly developing with no larval dispersal and among these there is evidence of strong local adaptation forming distinct ecotypes in contrasting habitats by parallel evolution. In at least one of the directly developing species (L. saxatilis) divergent selection among ecotypes has resulted in partial reproductive barriers that further impede gene flow among ecotypes. Furthermore, convergent evolution among species has produced superficially similar morphs in different habitats. Ecotype formation, ecological reproductive barriers and convergence among species all indicate that ecological processes are critical for evolution of Littorina species. D 2002 Elsevier Science B.V. All rights reserved.