Polymorphic shell banding in the dog-whelk, Nucella lapillus (Mollusca)

The shell of the Common dog-whelk (Nucella lapillus (L.)) is white and unbanded at most places around the British Isles. However, high frequencies of banding occur on the Buchan coast, around Anglesey and the Menai Straits, on the Cower Peninsula, around the Devon–Somerset border in the Bristol Channel, and especially on the north Cornish coast (reaching a peak between Newquay and Padstow). The frequency of banding is significantly less in older than younger whelks in the same locality, and this change is uncorrelated with the selection against shell shape variation that takes place on exposed shores. It is concluded that banding is a pleiotropic manifestation of physiological variation, and that a study of such variation in different morphs could indicate the importance of different physiological stresses at different stages of the life history of N. lapillus.     

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.     

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 colour variation in Littorina saxatilis Olivi (Prosobranchia: Littorinidae): a multi-factor approach

The marine snail Littorina saxatilis is highly polymorphic for shell colour. It lives in the heterogeneous intertidal zone, where there are sharp transitions in a number of abiotic factors that may influence the relative fitness of morphs. We investigated the hypothesis of selected variation by relating the colour distribution to five factors (wave exposure, substratum, shore level, sex, snail age), and to interactions between them. We compared patterns from geographical areas in Sweden, Iceland and Russia. Cryptic morphs (tessellated and different dark colours) generally dominated (80–98%) while conspicuous morphs (white, yellow, red and banded) were less common (2–20%). The colour frequencies were often related to wave exposure, substratum and shore level. Frequencies rarely varied with age and never with sex. In order to test the assumption that the different colours are genetically determined we cross-bred snails from Iceland in the laboratory. Both the presence of bands and the ground colours of the shell were inherited, and we have tentative support for a one-locus two-allele model for banding. Our results support a model of selected inherited colour variation, involving a number of different selective agents, the importance of which may vary between populations on local and geographical scales.     

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.     

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.     

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.     

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.     

Some observations on shell-shape variation in North American populations of Nucella lapillus (L.)

This paper considers shell-shape variation in samples of the dog-whelk/dog-winkle, ucella lapillus , from the southern half of its North American range, between 41 and 46N, and compares it with the pattern seen in Europe. At the extreme southern limit of its American range, to the south of Cape Cod, the species exhibits features to be expected in an animal close to an environmental limit. It is generally rare and has a patchy distribution. There is little variation in the shell: almost all adult individuals have rather large, thick, white, elongated shells. This contrasts sharply with the situation in Portugal, at the southern limit in Europe, where the animals have small thin, coloured shells of intermediate shape.
Away from the marginal situation, north of Nahant (42^CN) in America, the species shows much the same range of variability in shell size, shape and colour on both sides of the Atlantic. Most populations appear to show the same pattern of shape variation in asociation with the exposure of their habitat to wave action. Animals from exposed sites tend to have shorter, squatter shells than their compatriots in shelter. However, in America as in some parts of Europe, there are occasional enclaves which do not fit the usual pattern. It is interesting to note that the form normally associated with extremely exposed shores from Brittany to Faroe in Europe is found in Atlantic Canada but is apparently absent from southern populations in both the U.S.A and the Iberian Peninsula.     

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.     

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.     

Temporal morph frequency changes in sand‐dune populations of Cepaea nemoralis (L.)

Changes in morph frequency over time in sand‐dune populations of Cepaea nemoralis in the British Isles have been examined using the Evolution Megalab database. Frequencies in colonies on a sand dune at Berrow, Somerset were estimated in 2008–9. This extends a survey started in 1926 by A. E. Boycott and C. Diver and continued in the mid‐20th Century by B. C. Clarke and J. J. Murray. An increase in the frequency of the mid‐banded morph, noted in earlier work, has continued. The apparent decrease in brown was not confirmed but the yellow frequency has increased. At a range of dunes in the British Isles, comparisons between data from the mid‐20th Century and the early 21st Century indicate an increase in yellow and mid‐banded morphs and a decrease in banding and brown morphs. These results differ from the overall trends derived from Europe‐wide comparison of early data with Evolution Megalab data, in which banded and mid‐banded increased in frequency, whereas there was no overall change in yellow. The general pattern of regional variation has been retained, although there is also high heterogeneity between samples, suggesting that a variety of factors are involved in explaining the changes. The mean shifts in frequency are consistent with climatic change over the period. Dunes are probably the most likely habitat in which to detect such a change. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 108 , 315–322.     

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.     

Biogeography and designatable units of <Emphasis Type="Italic">Bombus occidentalis</Emphasis> Greene and <Emphasis Type="Italic">B. terricola</Emphasis> Kirby (Hymenoptera: Apidae) with implications for conservation status assessments

Conservation action for species of concern requires that “designatable units” (e.g., species, subspecies, geographic races, genetically distinct forms) are clearly defined, or that the species complex is treated as a whole. Several species of bumble bee are currently threatened, and some of these have cryptic colouration (resembling other species), or form complexes that vary considerably in colour patterning. Here we address the taxonomy and distribution of Bombus occidentalis Greene and B. terricola Kirby, both of which are currently of conservation concern in North America. Bombus occidentalis includes two apparently monophyletic groups of COI barcode haplotypes (recently considered as subspecies) with ranges mostly separated by that of their sister species, B. terricola. The southern B. o. occidentalis ranges throughout the western United States and into western Canada from southern Saskatchewan and Alberta, and throughout British Columbia north to ca. 55°N; the northern B. o. mckayi Ashmead, is restricted to north of this in British Columbia, westernmost Northwest Territories, Yukon Territory and Alaska. Bombus o. mckayi exists, as far as is known, only with a “banded” colour pattern. By contrast, B. o. occidentalis occurs in both banded and non-banded colour patterns, although the southern banded colour pattern is geographically isolated from the northern subspecies. Bombus o. occidentalis has declined throughout its range, perhaps due in part to exposure to novel parasites. Despite having similar levels of parasitism (ca. 40 %) as the southern subspecies, B. o. mckayi appears to have stable populations at present. There is therefore compelling evidence that the two subspecies should be distinguished for conservation and management purposes. We present the evidence for their distinction and provide tools for subspecies recognition.     

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.     

Distribution patterns of morph frequencies in the snail Cepaea hortensis in Iceland

In Iceland Cepaea hortensis Müll. reaches its northern limit of distribution occurring in restricted areas along the south coast. Samples of snails collected along steep cliffs in two such restricted areas were effectively monomorphic for shell colour (yellow), but were polymorphic for banding pattern and revealed strong area effects. In both localities samples from sites facing east contained varying frequencies of unbanded snails whereas in ecologically similar sites facing south unbanded were absent. In an experimental population released at a south-facing site unbanded snails failed to become established whereas banded individuals survived and bred. It is suggested that the area effects are maintained through non-visual (most likely climatic) selection though other possibilities cannot be ruled out.     

Clines revisited: The timing of pupping in the harbour seal (Phoca vitulina)

The regional variation in the pupping season of the harbour seal ( Phoca vitulina ) was reviewed using the birth periods reported for 65 colony sites distributed over a range from 30.4 to 78.5 North latitude. The birth timing of P. v. vitulina was not related to latitude, but birthing in P. v. concolor along eastern North America exhibited a latitudinal cline. The timing of birth in P. v. richardsi varied in three distinct patterns: (1) a significant unidirectional latitudinal cline extending between Baja California and the west coast of Washington; (2) a cluster comprised of Puget Sound, Washington and Vancouver Island, British Columbia colonies in which birthing occurred an average of 65 days later than on the Washington coast; and (3) a cluster from northern British Columbia and Alaska which did not demonstrate a latitudinal cline. Insufficient data were available for the analysis of P. v. mellonae or P. v. stejnegeri .
We found great regional variation in the timing of birth among all colonies, with mean birth dates occurring as early as 15 March and as late as 3 September. Little variation existed north of 50. To the south of 50, however, most of the variation could be attributed to correlation with latitude or to affiliation with the Puget Sound, Washington-Vancouver Island, British Columbia geographic area.
Clinal variation in pupping could result from: (1) geographic variations in a selective factor with perhaps gene exchange between contiguous populations playing a role in smoothing the variation; or (2) for populations between Mexico and the west coast of Washington, regional variation in a non-selective environmental variable, such as photoperiod.     

Precise tuning of barnacle leg length to coastal wave action

Both spatial and temporal variation in environmental conditions can favour intraspecific plasticity in animal form. But how precise is such environmental modulation? Individual Balanus glandula Darwin, a common northeastern Pacific barnacle, produce longer feeding legs in still water than in moving water. We report here that, on the west coast of Vancouver Island, Canada, the magnitude and the precision of this phenotypic variation is impressive. First, the feeding legs of barnacles from protected bays were nearly twice as long (for the same body mass) as those from open ocean shores. Second, leg length varied surprisingly precisely with wave exposure: the average maximum velocities of breaking waves recorded in situ explained 95.6-99.5% of the variation in average leg length observed over a threefold range of wave exposure. The decline in leg length with increasing wave action was less than predicted due to simple scaling, perhaps due to changes in leg shape or material properties. Nonetheless, the precision of this relationship reveals a remarkably close coupling between growth environment and adult form, and suggests that between-population differences in barnacle leg length may be used for estimating differences in average wave exposure easily and accurately in studies of coastal ecology.     

Genetics of polymorphism in the land snail,Cepaea nemoralis

The results of 40 single-pair matings of the landsnailCepaea nemoralis, mostly concerning the rarer banding patterns are presented. A total of 3678 F₁ individuals were obtained, 2315 of which were scored when adult, the remainder as juveniles.The presence or absence of band 3 in banded snails does not seem to be genetically determined. It is shown that several banding patterns (e.g. 12300, 02300, 00340, 003300, 00305) should be classified as 00300. The presence or absence of extra (satellite-) bands seems to be multifactorially controlled. It is suggested that pattern 10345 is dominant over 12345 and that it is determined either by an allele of the threebanded locus, recessive to pattern-allele 00345, or by a different locus but then epistatically suppressed by the gene for 00345. Pattern 02345 in some cases is genetically 00345 and in other cases 12345. Fusion of bands 4 and 5 is multifactorially controlled, and is perhaps influenced by, or linked to, the loci for colour and three-bandedness. Fusion of bands 1 and 2 seems to be also multifactorially controlled. This fusion is strongly correlated with fusion (45), and is independent of colour. Pale is recessive to dark body colour. The latter occurs in several shades which are multifactorially controlled. Reddish body colour is recessive to yellowish, and the gene concerned is linked with that for shell colour. Variation in the expression of dominance was found at the loci for 00300, 00345, 10345, reddish body colour and pale body colour.