Visible variation in the dog-whelk, Nucella lapillus

Shell shape and colour variation is common in littoral molluscs. As far as shape is concerned, exposure to wave action acts as a strong agent of natural selection, but only speculation seems to have been directed towards elucidating the determinants of colour variation. In the dog-whelk ( Nucella lapillus (L.)) diet may play some part in producing the pigment for colour. However white and banded forms are often found in otherwise coloured colonies. This study describes the classification for colour and banding of 83,524 whelks from 444 areas around the British Isles and west Atlantic coast. Colour and banding were significantly correlated r =0.45±0.05). Because of the possible involvement of diet in shell colour, attention has been confined to banded forms. No obvious pattern in distribution could be discerned. Possible factors affecting the occurrence and incidence of banding are: climate; geology; exposure to wave action; predation; intra- or interspecific competition; cryptic genetical factors; or intraspecific recognition. The only one which was definitely associated with banding frequency was exposure ( r = 0.33±0.05), but there were so many exceptions to the correlation (e.g. highly exposed populations which were entirely unhanded), that this is unlikely to be causal. The most probable explanation seems to be the local spread of mutant forms (probably linked to fitness traits), which have not attained equilibrium frequencies–even though N. lapillus has apparently occurred in large colonies round much of the British coast since the end of the Pleistocene.     

Some observations on shell shape variation in Pacific Nucella

This paper considers the patterns of shell shape variation shown by Nucella canalicuata, N. emarginata and N. lamellosa from two areas of the Pacific Northwest: the shores near Friday Harbour on San Juan Island and near Bamfield on the west coast of Vancouver Island. No clear pattern of variation in association with changes in exposure was seen in either N. canaliculata or N. lamellosa . It appears that genetic influences are more important controls of shell shape than environmental selection in both these species. Nucella emarginata shows the nearest approximation to the pattern shown by the Atlantic species, N. lapillus , but only at the exposed end of the wave-action gradient. On those shores, enclaves from the most surf-washed open coast headlands have shells with proportionally larger apertures (and thus a shorter, squatter form) than their equivalents in local shelter. But, unlike in N. lapillus , the trend does not continue onto genuinely sheltered shores. Under these circumstances the species is generally rare and, where enclaves do occur, their shells are of much the same shape (although of a much larger size) as in more exposed situations.     

Phenotypic variation along a cline in allozyme and karyotype frequencies, and its relationship with habitat, in the dog-whelk Nucella lapillus, L.

The dog-whelk Nucella lapillus exhibits a number of phenotypic variations and genetic polymorphisms which correlate with habitat-specific environmental pressures, especially those associated with wave action and temperature. This study investigates the relationship between genetic composition (karyotypic and electrophoretic variation) and phenotypic differentiation in N. lapillus sampled at 15 points along an 8 km stretch of coastline. Coincident clinal variation in gene frequencies and shell shape is described; they covary with differences in karyotype and also with growth. Laboratory-reared young show that differences in phenotype (shell shape and growth) are inherited. Experimental evidence is presented that specific shell shapes are adaptive under conditions of thermal stress. Together with the well-established correlations between shell shape and shore exposure, this association provides an argument for a relationship between genetic composition, phenotype and habitat in this species.     

Shell shape variation in dog-whelks (Nucella lapillus (L.)) from the West Coast of Scotland

European populations of the common dog-whelk, Nucella lapillus (L.), usually show a neat and precise pattern of shell shape variation with the exposure of their habitat to wave action. Whilst this is the case along much of the west coast of Scotland, there are a number of instances where unusually elongated shells occur, somewhat reminiscent of the form described for the Severn Estuary. There are no obvious environmental or geographical correlates to explain the occurrence of these forms and a genetical interpretation is sought.     

Observations on the biology of the trochid gastropod Austrocochlea constricta (Lamarck) (Prosobranchia). I. Factors affecting shell-banding pattern

The intertidal trochid gastropod Austrocochlea constricta (Lamarck) has a variable pattern of banding, the shell ranging from white with fine black stripes, to completely black. The patterns may be classified into six arbitrarily chosen types. Populations were studied on three shores chosen to represent the range of habitat of the species (from estuarine to open coast localities) to determine the relative importance of environmental factors on shell-banding. The densities and proportions of the population in different stripe-classes were estimated from quadrat samples on the three shores. Analysis of size-frequency distributions indicates recruitment to be continuous. In all months, juveniles were at greater densities at the upper level of the distribution of the species on open coast and estuary-mouth platforms; the estuarine population was uni modal in size-frequency distribution. Growth rates of caged animals were higher on the open coast than in the estuary, and changed in animals transferred between the two localities, but did not differ between animals of different banding pattern. The proportion of the population in each stripe-class was constant on each shore, suggesting large scale selection processes do not cause the observed differences in frequencies of each banding pattern.The concentrations of the major shell pigment, uroporphyrin I, varied between stripe-classes and, within classes, between shores, with a trend for more densely pigmented shells on the open coast, a trend also evident for the proportion of the population in the darker stripe-classes. Caged animals transferred from the open coast to the estuary showed changes in banding pattern which were consistent with the differences in pigmentation of the two populations. Animals transferred from the estuary to the open coast changed pattern at the same frequency as controls from the open coast; a result of severe storms which caused the open coast population to show changes of banding pattern.It is concluded that shell-banding patterns in A. constricta are primarily governed by environmental factors.     

An ancient transpecific polymorphism shows extreme divergence in a multitrait cline in an intertidal snail (Nucella lapillus (L.))

Clines in intraspecific genetic variation are frequently associated with an environmental transition. Here, divergence among nucleotide sequences of two nuclear loci, cytosolic and mitochondrial malate dehydrogenase (cMDH and mMDH, respectively), is described, in a multitrait cline over a distance of ca. 3 km where shell phenotype, allozyme, mitochondrial DNA haplotype, and centric fusion (Robertsonian translocations) frequencies covary with temperature and humidity and change abruptly in a continuous population of the dog-whelk (Nucella lapillus), a common intertidal snail of the north temperate Atlantic. Protein electrophoresis has already shown two alleles of mMDH varying from fixation of one allele to near fixation of the other, whereas cMDH appears to be monomorphic. The results of this study show a striking disparity in nucleotide sequence divergence among alleles at the two loci, with extreme molecular differentiation in one of them. Four alleles of cMDH were found to have nucleotide and amino acid sequence divergences of 0.4% and 0.3%, respectively. In contrast, the two mMDH cDNA alleles differed by 23% and 20% at the nucleotide and amino acid levels, respectively. Analysis of a 91-bp partial nucleotide sequence of mMDH from Nucella freycineti, the closest relative of N. lapillus, revealed two similar alleles and indicated that the divergence in mMDH in N. lapillus represents an ancient transpecific polymorphism in these Nucella. Together with earlier studies on variation in N. lapillus, it is argued that the polymorphism in mMDH and the clines in N. lapillus represent the presence of two persistent coadapted gene complexes, multitrait coevolving genetic solutions to environmental variation, which may presently enable this snail to exploit a diverse environment successfully.     

Variation in mitochondrial DNA in a cline of allele frequencies and shell phenotype in the dog-whelk Nucella lapillus (L.)

Genetic constitution in the intertidal gastropod Nucella lapillus (L.) influences shell shape, growth rate and physiology. Clinal variation in these traits along a 5 km stretch of coastline in south Devon can be related to environmental variation in temperature and desiccation stress. We have examined mtDNA variation along this shore to investigate whether the cline represents primary or secondary contact. Two distinct mtDNA haplotypes were found which exhibit coincident step clines with karyotypic, allozymic and phenotypic variation and covary with the environmental pressures of temperature and desiccation. These results are interpreted in the context of the wider scale distribution of genetic and phenotypic variation in N. lapillus. It is suggested that the shore studied may represent one of a number of regions of secondary contact within a mosaic hybrid zone in N. lapillus , where coadapted phenotypic variation correlates with habitat and the position of the clines represents an environmental transition.     

Otolith microstructure of Japanese sea bass larvae and juveniles: interpretation and utility for ageing

This paper interprets and discusses the usefulness of otolith microstructure for ageing Japanese sea bass ( Lateolabrax japonicus ) larvae and juveniles. Samples were collected from the Tango Sea along the Japan Sea coast, January–March 2007. Known-age (0-day and 10-day-old) larvae were obtained from the Ibaragi Prefectural Hatchery, Japan. Sagittal and lapillar otolith were processed and read using an otolith reading system. Clearly discernible hatch- and first-feeding marks were evident on sagitta, and development of accessory premordia (AP) appeared to be associated with larva-juvenile transition; however, no other marks indicating metamorphosis or settlement were evident. In lapillus, no discernible check mark was found. Known-age larvae showed that deposition of the first daily increment (DI) corresponded to first-feeding, which occurred at day-4 post-hatch. However, mean increment counts were significantly lower in lapillus than in sagitta, caused by poorly expressed increments around the centrum as well as relatively unclear centrum of the lapillus. The authors suggest that the use of lapillus can cause significant underestimation of age. Therefore, the sagitta is recommended for age and growth estimations of larvae and juveniles, although the presence of numerous subdaily increments warrants careful preparation and interpretation of the microstructure. A test for asymmetry showed the right and left otoliths to be quite symmetrical and their DI counts not significantly different, suggesting that either otolith can be used for studying age and growth of Japanese sea bass larvae and juveniles.     

Resistance to shell breaking in two intertidal snails

The ability of shells to withstand shell breaking forces has been examined in two intertidal prosobranchs, Nucella lapillus and Littorina littorea , using four methods: measuring shell strength on a compressive testing machine, measuring the shell to body mass ratio, measuring the shell thickness and measuring the ability of crabs to break shells in aquarium experiments. Nucella lapillus consistently showed a relationship between shell vulnerability and environmental variables: the shells were easier to break at sites where rock and boulder movement was the least. Although some between-site differences were found in L. littorea shells, these were less than in N. lapillus and did not relate to environment variables: the shells were easier to break at sites where exposure to wave action was the least. Although some between-site differences were found in L. littorea shells , these were less than in N. lapillus and did not relate to environmental factors. However, both species appear to grow into a size refuge in which they are secure from predation by shore crabs at the sites where these crabs are commonest.     

A multivariate study of geographic variation in the whelk Dicathais

An analysis has been made of the variation in shell shape and shell characteristics of 889 Australian and New Zealand specimens of the genus Dicathais, using multivariate techniques. Shell measurements taken were: the overall length, length of spire, length of aperture, and width of aperture. Weight of the shell plus the preserved animal was also recorded. The sculpture of the shell, thickness of the lip, and the presence or absence of a reddish or purplish colouration or banding on the inside of the lip, were assessed qualitatively.Principal component analyses of the size measurements for each site showed that the first principal component, which accounted for greater than 95% of the variation at each site, was associated with variation in the ‘size’ of the animal. Canonical analysis of the size measurements showed a cline in shell shape from the animals on the western side of Australia to those on the eastern side of Australia and New Zealand. The resulting canonical variates were associated with variation in the ‘shape’ of the shell. Principal component analyses of the between-group matrix and of the within-group matrix of the size measurements showed that the site means exhibited a similar pattern of dispersion to that of the animals within each site.Canonical analysis of the shell characteristics showed that variation along the first canonical axis was largely produced by shell sculpture, while variation along the second resulted from differences in colouration/banding.The generalized variances of the correlation matrices for the size measurements showed that groups with similar shell shape were associated with the presence of granite substrata and/or mussel beds or, alternatively, with limestone substrata, but canonical correlation analysis of the relationship between the size measurements and shell characteristics showed that no consistent trend was evident over all sites.A subjective examination of the structure of the radula of 84 animals showed that two distinct morphological forms were present, but that they were not correlated either with sex or any of the named shell forms or site groupings.An analysis of the growth curves of 27 animals of the two forms from the eastern and western coasts of Australia, held in the laboratory, was carried out. The eastern coast form showed a loss of sculpturing and a change in shell shape when kept under west coast conditions and on a mussel diet.Water temperature, diet, substratum, and degree of exposure to wave action were all found to show associations with variations in either shell shape or shell characteristics. It is suggested that the selective force of the habitat which produces changes in shell shape and shell characteristics of the animals at any site is a complex of factors, many of which are interrelated. The genetic basis for the development of shell shape and production of the shell characteristics in Dicathais may be similar to that found in Nucella lapillus (L.) in the Northern Hemisphere.These data suggest that the Dicathais found at the sites studied in this investigation are all part of the same ‘population’, the shell shape and shell characteristics of the adult populations being determined both by selection and phenotypic expressions caused by the selective force of the habitat at each site. It is concluded that the genus consists of a single highly variable species.The value of the application of multivariate analyses to this type of study is shown to lie in the way in which the techniques provide an overall picture of the variation within sites and of the variation between sites.     

Quantitative measures and 3D shell models reveal interactions between bands and their position on growing snail shells

The nature of shell growth in gastropods is useful because it preserves the ontogeny of shape, colour, and banding patterns, making them an ideal system for understanding how inherited variation develops, is established and maintained within a population. However, qualitative scoring of inherited shell characters means there is a lack of knowledge regarding the mechanisms that control fine variation. Here, we combine empirical measures of quantitative variation and 3D modeling of shells to understand how bands are placed and interact. By comparing five‐banded Cepaea individuals to shells lacking individual bands, we show that individual band absence has minor but significant impacts upon the position of remaining bands, implying that the locus controlling band presence/absence mainly acts after position is established. Then, we show that the shell grows at a similar rate, except for the region below the lowermost band. This demonstrates that wider bands of Cepaea are not an artifact of greater shell growth on the lower shell; they begin wider and grow at the same rate as other bands. Finally, we show that 3D models of shell shape and banding pattern, inferred from 2D photos using ShellShaper software, are congruent with empirical measures. This work therefore establishes a method that may be used for comparative studies of quantitative banding variation in snail shells, extraction of growth parameters, and morphometrics. In the future, studies that link the banding phenotype to the network of shell matrix proteins involved in biomineralization and patterning may ultimately aid in understanding the diversity of shell forms found in molluscs.     

Variation in dog-whelk shells in relation to wave action and crab predation

In Nucella lapillus there is usually a progressive gradation in mean shell shape from short squat individuals on exposed headlands to more elongated ones in shelter. This pattern has been attributed to the differential selective effects of wave action and crab predation, although it would almost certainly be an oversimplification to imagine these as the only significant forces involved, especially near the limits of the species' distribution.
However, whilst this pattern of shell-shape variation with exposure is generally true over most of the animal's range in both Europe and North America, there are exceptions. There are occasional enclaves with much more elongated shells than would normally have been expected. Sometimes these are so abundant, as in the Severn Estuary, that all dog-whelk enclaves are unusually elongated, regardless of the exposure of their habitat.
In other areas, such as south-eastern England, the Solway Firth and the area around the mouth of the Conway the shells are not unusually elongated, but the enclaves show very little variation: a normal sheltered-shore form is seen wherever the species occurs. Shetland samples appear to be a combination of this pattern (predominating) with the 'normal' one showing the full range of shellshape variation.
Nucella appears in the Atlantic fossil record at the end of the Pliocene without any antecedent forms. It is assumed to have colonized from the Pacific and exploited the vacant niche before the onset of the Ice Age. Successive advances and retreats of the ice, with attendant changes in sea level, will have served to break up and recombine those dog-whelk populations that were not eliminated. It is postulated that the modern Nucella lapillus is a combination of several genetically distinct populations, some of which show the full range of variation and may respond to the selective effects of crabs and waves, and some of which do not and show little variation.     

Corrigendum

A re-evaluation of shell shape variation in Shetland dog-whelks.Mucelbi lapillus (I.) and their use as biological exposure indicators.Journal of Molluscan Studies.58: 315–328. Figure 6 and Figure 9 arc transposed. The caption of Figure6 is correct, but the illustration is that of Figure 9 and viceversa.     

Two different patterns of shell-shape variation in the dog-whelk Nucella lapillus (L.)

Populations of the common dog-whelk, Nucella lapillus (L.), usually show a gradation in mean shell shape related to the exposure of the shore on which they live. Enclaves from exposed headlands have shorter, squatter shells than do their compatriots in shelter. This paper describes the pattern of shell-shape variation shown by populations in the Isles of Scilly and on the north coast of Wales. In both places a gradation is present, but it is not numerically similar, the Welsh population being more elongated. It is concluded that the selective agents are the same in both places. Wave action always eliminates the most elongate-shelled whelks first, and crabs always find it easier to take the animals with the widest apertures to their shells. The reason for the observed differences between the patterns described here lies in the genetic differences between the populations: Scillonian whelks do not have the option of being as elongated as the Welsh ones, which, in turn, cannot show very short squat shells in exposure.     

Shell-shape variation in Faroese dog-whelks (Nucella lapillus (L.))

Nucella lapillus is a common and widely distributed carnivorous gastropod of North Atlantic rocky sea shores. Populations of this animal usually show variation in shell shape according to the exposure of their habitat to wave action, with individuals from exposed sites having a short squat shell and a wide aperture as compared with a more elongated form seen in shelter. The same pattern of variation is seen over most of the species European range, but there are some exceptions. One of these has been described in Sullom Voe (Shetland) and this prompted an investigation of Faroese populations to ascertain whether they behaved in a similar manner. It is shown in this paper that Faroese populations vary in shell shape with exposure in the usual way (and not like those in Shetland) and moreover show such a fine and precise reflection of minor alterations in environmental conditions that measurement of dog-whelk shells may prove to be the best way of 'measuring' exposure in Faroe.     

Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

Hotter conditions favour effectively unbanded (EUB) shells in the snail Theba pisana. T. pisana is also polymorphic for colour of the shell's apex, determined by a pair of alleles at a locus linked to the banding locus. Apex colour is epistatic to shell banding, such that banded snails with a dark apex have darker bands. Annual censuses over 22 years across an ecotone between a sheltered Acacia thicket and open dune vegetation showed a persistent association of both EUB shells and pale apex with the Open habitat. The parallel variation was due partly to strong phenotypic disequilibrium, as the combination of EUB with dark apex was rare. Nevertheless, in fully banded shells the frequency of pale apex was also higher in the Open habitat, confirming independent, parallel associations of the two contributors to paleness. Within the Acacia habitat, temporal variation of the frequencies of banding morphs was much greater than for apex colour, and EUB shells were associated with hotter summers. Consistent with its primary effect only on the very small snails, apex colour did not vary with summer conditions, but instead, higher frequencies of pale apices were associated with sunnier winters. The intensity of selection was lower on apex colour than shell banding, due partly to the constraint of phenotypic disequilibrium. The shell traits in T. pisana are an example of complex responses to climatic variation, in which phenotypic disequilibrium constrains evolution of apex colour, but separate mechanisms of selection are evident.     

Effects of copper and cadmium on cholinesterase and glutathione S-transferase activities of two marine gastropods (Monodonta lineata and Nucella lapillus)

With the view of using Nucella lapillus and Monodonta lineata as bioindicators in biomonitoring programs in the NW coast of Portugal, the sensitivity to copper and cadmium of these two common species in Atlantic coasts of Europe was investigated. Assays based on mortality and on the activity of the enzymes cholinesterases (ChE) and glutathione S-transferases (GST) were used, as these biomarkers have been used in biomonitoring studies in the area. ChEs present in foot muscle of both species were characterised and found to show properties of both typical acetylcholinesterase and pseudocholinesterase. Cadmium LC50s for N. lapillus and M. lineata were 2.64 and 2.44 mg/L, respectively, while the lowest observed effect concentration (LOEC) was 1.53 mg/L for both species. LOEC value for cooper was 0.075 mg/L for both. Cadmium in vivo exposure increased ChE activity of N. lapillus, but had no effects on M. lineata ChE. No in vitro effects of cadmium on ChE activity of any of the tested species was observed. Copper had no significant in vivo effects on ChE activity, although it inhibited the ChE of both species in vitro, the IC50s being 5.87 and 12.17 mg/L for N. lapillus and M. lineata, respectively. Cadmium had no significant effects on GST activity of either species, while copper caused a significant reduction of N. lapillus GST (LOEC=0.044 mg/L) but had no effect on M. lineata GST. Results indicate that (i) N. lapillus and M. lineata have a similar acute sensitivity to cadmium and copper; (ii) ChE and GST of these species are sensitive to cadmium (iii) ChEs of both species are inhibited by copper at concentrations in the mg/L range and therefore, its use is limited to heavily polluted sites; (iv) N. lapillus GST does not seem to be a suitable biomarker for copper, at least in the range of concentrations tested, since it was inhibited by copper, but no clear concentration-response relationship was observed.     

Physiological variation in the dog-whelk Nucella lapillus, L. either side of a cline in allozyme and karyotype frequencies

Genetic constitution in the intertidal gastropod Nucella lapillus influences variation in shell shape and growth rate which in turn are correlated with such habitat variables as wave action and temperature. We have investigated the response to hyperosmotic stress of samples from a cline in karyotype and allozyme frequencies and shell shape. Animals with a shell shape associated with environments where temperature and desiccation stress are important respond less to hyperosmotic stress than animals living in a high wave energy environment. With regard to the interaction between shell shape, physiology and habitat, animals with elongate shells associated with protected shores are shown to exhibit a reduced response to hyperosmotic stress compared to animals with a more spherical shell shape; this is discussed in relation to the production of an adaptive phenotype.     

Scale-dependence in geographic variation in a freshwater gastropod across the Palearctic

ABSTRACT

The reality of spatial clinal variation in morphological traits of freshwater pulmonate snails (Gastropoda: Pulmonata) has repeatedly been questioned or totally discounted. There is a lack of sound statistical evidence in the articles hitherto published on this subject supporting these claims. Here, by means of different analytical methods (analysis of spatial autocorrelation, linear regression analysis, canonical correlation analysis and others), we demonstrate that shell variation in the dwarf pond snail, Galba truncatula, is patterned in space throughout the northern and central Palearctic, with latitudinally-oriented clines in body size and in some shell proportions. Shell size in G. truncatula decreases with latitude and temperature, representing a special case of converse Bergmann cline. However, the temperature itself is hardly the main driver of shell size variation. It is argued that the shorter growing seasons at high latitudes may represent a better explanation for the observed trend. Shell proportions in the dwarf pond snails vary weakly at the macrogeographic scale, being spatially patterned at lower (mesogeographic) scales around 1200–1500?km. In general, spatial variation in G. truncatula shell size is decoupled from variation in shell shape, demonstrating clear scale-dependence similar to that found in different species of terrestrial (non-aquatic) pulmonate snails.