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Concept: Gastropod shell


While components of the pathway that establishes left-right asymmetry have been identified in diverse animals, from vertebrates to flies, it is striking that the genes involved in the first symmetry-breaking step remain wholly unknown in the most obviously chiral animals, the gastropod snails. Previously, research on snails was used to show that left-right signaling of Nodal, downstream of symmetry breaking, may be an ancestral feature of the Bilateria [1, 2]. Here, we report that a disabling mutation in one copy of a tandemly duplicated, diaphanous-related formin is perfectly associated with symmetry breaking in the pond snail. This is supported by the observation that an anti-formin drug treatment converts dextral snail embryos to a sinistral phenocopy, and in frogs, drug inhibition or overexpression by microinjection of formin has a chirality-randomizing effect in early (pre-cilia) embryos. Contrary to expectations based on existing models [3-5], we discovered asymmetric gene expression in 2- and 4-cell snail embryos, preceding morphological asymmetry. As the formin-actin filament has been shown to be part of an asymmetry-breaking switch in vitro [6, 7], together these results are consistent with the view that animals with diverse body plans may derive their asymmetries from the same intracellular chiral elements [8].

Concepts: DNA, Gene, Gene expression, Animal, Symmetry, Mollusca, Gastropod shell, Snail


BACKGROUND: Various shapes of gastropod shells have evolved ever since the Cambrian. Although theoretical analyses of morphogenesis exist, the molecular basis of shell development remains unclear. We compared expression patterns of the decapentaplegic (dpp) gene in the shell gland and mantle tissues at various developmental stages between coiled-shell and non-coiled-shell gastropods. RESULTS: We analyzed the expression patterns of dpp for the two limpets Patella vulgata and Nipponacmea fuscoviridis, and for the dextral wild-type and sinistral mutant lineage of the pond snail Lymnaea stagnalis. The limpets had symmetric expression patterns of dpp throughout ontogeny, whereas in the pond snail, the results indicated asymmetric and mirror image patterns between the dextral and sinistral lineages. CONCLUSION: We hypothesize that Dpp induces mantle expansion, and the presence of a left/right asymmetric gradient of the Dpp protein causes the formation of a coiled shell. Our results provide a molecular explanation for shell, coiling including new insights into expression patterns in post-embryonic development, which should aid in understanding how various shell shapes are formed and have evolved in the gastropods.

Concepts: Gene, Developmental biology, Mollusca, Gastropod shell, Snail, Gastropoda, Lymnaea stagnalis, Limpet


Dispersal has received growing attention in marine ecology, particularly since evidence obtained with up-to-date techniques challenged the traditional view. The dogwhelk Nucella lapillus L., a sedentary gastropod with direct development, is a good example: dispersal was traditionally assumed to be limited until studies with microsatellites disputed this idea. To shed some light on this controversy, the genetic structure of dogwhelk populations in northwest Spain was investigated with highly polymorphic AFLP markers giving special attention to the influence of hydrodynamic stress. In agreement with the expectations for a poor disperser, our results show a significant genetic structure at regional (<200 km) and areal scales (<15 km). However, the spatial genetic structure varied with wave-exposure in the present case study: IBD was evident under sheltered conditions but absent from the exposed area where genetic differentiation was stronger. Our results provide evidence that differences in wave-exposure can exert a detectable influence on the genetic structure of coastal organisms, even in species without a planktonic larva.

Concepts: DNA, Biology, Population, Mollusca, Dog whelk, Amplified fragment length polymorphism, Nucella, Gastropod shell


Autotomy of body parts offers various prey animals immediate benefits of survival in compensation for considerable costs. I found that a land snail Satsuma caliginosa of populations coexisting with a snail-eating snake Pareas iwasakii survived the snake predation by autotomizing its foot, whereas those out of the snake range rarely survived. Regeneration of a lost foot completed in a few weeks but imposed a delay of shell growth. Imprints of autotomy were found in greater than 10 per cent of S. caliginosa in the snake range but in only less than 1 per cent out of it, simultaneously demonstrating intense predation by the snakes and high efficiency of autotomy for surviving snake predation in the wild. However, in experiments, mature S. caliginosa performed autotomy less frequently. Instead of the costly autotomy, they can use defensive denticles on the inside of their shell apertures. Owing to the constraints from the additive growth of shells, most pulmonate snails can produce these denticles only when they have fully grown up. Thus, this developmental constraint limits the availability of the modified aperture, resulting in ontogenetic switching of the alternative defences. This study illustrates how costs of adaptation operate in the evolution of life-history strategies under developmental constraints.

Concepts: Lung, Predation, Mollusca, Gastropod shell, Snail, Snake, Pulmonata, Freshwater snail


Snails are highly unusual among multicellular animals in that they move on a layer of costly mucus, leaving behind a trail that can be followed and utilized for various purposes by themselves or by other animals. Here we review more than 40 years of experimental and theoretical research to try to understand the ecological and evolutionary rationales for trail-following in gastropods. Data from over 30 genera are currently available, representing a broad taxonomic range living in both aquatic and terrestrial environments. The emerging picture is that the production of mucus trails, which initially was an adaptation to facilitate locomotion and/or habitat extension, has evolved to facilitate a multitude of additional functions. Trail-following supports homing behaviours, and provides simple mechanisms for self-organisation in groups of snails, promoting aggregation and thus relieving desiccation and predation pressures. In gastropods that copulate, trail-following is an important component in mate-searching, either as an alternative, or in addition to the release of water- or air-borne pheromones. In some species, this includes a capacity of males not only to identify trails of conspecifics but also to discriminate between trails laid by females and males. Notably, trail discrimination seems important as a pre-zygotic barrier to mating in some snail species. As production of a mucus trail is the most costly component of snail locomotion, it is also tempting to speculate that evolution has given rise to various ways to compensate for energy losses. Some snails, for example, increase energy intake by eating particles attached to the mucus of trails that they follow, whereas others save energy through reducing the production of their own mucus by moving over previously laid mucus trails. Trail-following to locate a prey item or a mate is also a way to save energy. While the rationale for trail-following in many cases appears clear, the basic mechanisms of trail discrimination, including the mechanisms by which many snails determine the polarity of the trail, are yet to be experimentally determined. Given the multiple functions of trail-following we propose that future studies should adopt an integrated approach, taking into account the possibility of the simultaneous occurrence of many selectively advantageous roles of trail-following behaviour in gastropods. We also believe that future opportunities to link phenotypic and genotypic traits will make possible a new generation of research projects in which gastropod trail-following, its multitude of functions and evolutionary trade-offs can be further elucidated.

Concepts: Evolution, Phenotype, Sex, Mollusca, Gastropod shell, Snail, Gastropoda, Gastropods


The gills, or ctenidia, of marine gastropods serve as the sites for respiratory gas exchange. Cilia on the surface provide the pump that moves water through the mantle cavity and enhance diffusion. Because the gills are housed inside the shell, it is difficult to view them while they are functioning. Published images of gills show contracted, fragile structures that are distorted by the processes of dissection and preservation. Members of the families Fissurellidae (keyhole limpets) and Haliotidae (abalone) have openings in their shells through which water enters and/or exits. I inserted an endoscope connected to a video camera into the openings of the shells of living, non-anaesthetized individuals of the fissurellid Diodora aspera and the haliotid Haliotis rufescens. In both species, the dorsal afferent branchial vessel of the afferent gill axis appeared large and inflated, as did the leaflets that extended from either side of the axis. In D. aspera, the leaflets appeared to fill the mantle cavity and responded to touch, particles, and dye in the water by contracting quickly and slowly re-extending. In contrast, the gills of H. rufescens did not noticeably respond to disturbance. On the other hand, these gills showed a regular pattern of pleats that had not been described in the extensive anatomical literature of these common and economically significant animals. These results provide a novel view of the gastropod mantle cavity as a dynamic space filled by the gills, which divide the mantle cavity into distinct incurrent and excurrent chambers and produce a laminar flow of water through the cavity. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.

Concepts: Mollusca, Gastropod shell, Abalone, Gastropoda, Intertidal zone, Limpet, Fissurellidae, Red abalone


The iconic gastropod genus Cyphoma is commonly observed in the Caribbean, where it lives in association with various octocorallian hosts. Each species in the genus Cyphoma has a unique, characteristic mantle pattern and colouration, which separates the valid taxa. Because of its abundance and recognisability Cyphoma gibbosum has been used as a model organism in several studies concerning allelochemicals, reef degradation, and physical defence mechanisms. Molecular analyses based on four molecular markers (COI, 16S, H3 and 28S) for three Cyphoma species (C. gibbosum, C. mcgintyi, C. signatum) and an unidentified black morph, collected from three localities in the Caribbean, show that they represent morphological varieties of a single, genetically homogeneous species. This outcome is in agreement with previous anatomical studies. As a result C. mcgintyi and C. signatum are synonymised with C. gibbosum, which is a key result for future work using C. gibbosum as a model organism. The striking morphological differences in mantle pattern and colouration are hypothesised to be the result of one of three possible scenarios: rapid divergence, supergenes (including balanced polymorphism), or incipient speciation.

Concepts: DNA, Evolution, Biology, Organism, Species, Gastropod shell, Ovulidae, Cyphoma


A new species of Scutalus Albers, 1850 (Gastropoda: Bulimulidae), Scutalus chango sp. n., is described from a coastal area of northern Chile. Empty shells of this new species were found buried in sand and under boulders and rocks in the foothills of the Chilean Coastal Range at Paposo, Región de Antofagasta. This new species is distinguished from all other Chilean terrestrial snails by its slender shell with a flared and reflected aperture, and by the presence of a columellar fold. This is the first record of Scutalus in Chile, and the southernmost record for this endemic South American bulimulid genus. The presence of this species in Paposo highlights the need for further research and for conservation guidelines in coastal areas of northern Chile, which have comparatively high levels of biodiversity and endemism.

Concepts: Biodiversity, Species, South America, Mollusca, Gastropod shell, Argentina, Chile, Snail


The periwinkle Littorina saxatilis has repeatedly evolved both a small, fragile and globose “wave ecotype” confined to wave-swept shores and a large, robust and elongated “crab ecotype” found in nearby crab-rich but less-exposed shores. This phenotypic divergence is assumed to reflect, in some part, local adaptation to wave exposure, but this hypothesis has received incomplete experimental testing. Here, we report a test of the prediction that the wave ecotype has a higher capacity to resist water flow than the crab ecotype. We sampled snails along a crab-wave transect and measured their resistance to dislodgement in a high-speed water flume with water speeds that match those of breaking waves in a range of relevant field conditions. Snails from the wave environment were consistently more resistant to water flow than snails from the crab environment and high resistance was positively correlated with the surface area of the foot and the area of the outer aperture contour both relative to shell size, and to the extent of lateral shell compression. In a separate experiment, we found that snails raised in still water in a common garden showed higher resistance to water flow if originating from a wave environment than from a crab environment, and this was true both at juvenile (2 weeks) and adult (10 months) developmental stages. This result suggests genetic control of a distinct “wave adapted” phenotype, likely to be maintained under strong divergent selection between the two adjacent habitats.

Concepts: Gene, Natural selection, Evolution, Phenotype, Experiment, Gastropod shell, Adaptation, Littorina


Notodiscus hookeri is the only representative of terrestrial gastropods on Possession Island and exclusively feeds on lichens. The known toxicity of various lichen metabolites to plant-eating invertebrates led us to propose that N. hookeri evolved means to protect itself from their adverse effects. To validate this assumption, the current study focused on the consumption of two lichen species: Usnea taylorii and Pseudocyphellaria crocata. A controlled feeding experiment was designed to understand how the snail copes with the unpalatable and/or toxic compounds produced by these lichen species. The occurrence of two snail ecophenotypes, represented by a mineral shell and an organic shell, led to address the question of a metabolic response specific to the phenotype. Snails were fed for two months with one of these lichens and the chemical profiles of biological samples of N. hookeri (i.e., crop, digestive gland, intestine, and feces) were established by HPLC-DAD-MS and compared to that of the lichens. N. hookeri appears as a generalist lichen feeder able to consume toxic metabolite-containing lichens, independently of the ecophenotype. The digestive gland did not sequester lichen metabolites. The snail metabolism might be based on four non-exclusive processes according to the concerned metabolites (avoidance, passive transport, hydrolysis, and excretion).

Concepts: Evolution, Metabolism, Toxicity, Digestion, Mollusca, Gastropod shell, Snail, Gastropoda