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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Stabilizing selection in the dog-whelk (Nucella lapillus)

The amount of stabilizing selection undergone by a population of animals at different times of its life can be estimated by comparing the variances of different age samples. This paper describes an investigation into the intensities of selection experienced by populations of the common dog-whelk, Nucella lapillus (L.) exposed on different shores to different degrees of wave action. It was found that the variance of more exposed populations was reduced during life by up to 90%. There was a positive correlation between the intensity of stabilizing selection and the amount of wave action experienced by the whelks. Most of this selection took place during the first year or two of the life of the animals.     

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.     

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.     

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 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.     

The diet of the dog-whelk, Nucella lapillus (Gastropoda Prosobranchia)

The information at present available suggests that, when adult, Nucella lapillus may prey upon a considerable number of different species, but that the diet of recently hatched dog-whelks is rather more restricted. The food preferences of young Nucella have been investigated and it has been concluded that, while the diet of young and adult animals may differ to some extent, it is probably equally varied at all ages, and that cannibalism may be a frequent occurrence amongst all age groups.
It has been determined that the size of the prey influences the selective predation of Mytilus by Nucella. Dog-whelks show a marked preference for mussels in the 1 to 3 cm size range which may possibly be identified chemotactically.     

Allozyme differentiation of populations of the dogwhelk Nucella lapillus, (L.): the relative effects of geographic distance and variation in chromosome number

Geographic patterns of genie differentiation were compared with differentiation between karyotypes in the intertidal snail Nucella lapillus. Samples from 24 sites covering the species range in Europe and North America were analysed for allozyme variation at 16 soluble enzyme loci. Two homokaryotypes have been identified with diploid numbers 2n = 26 and 2n= 36 (variation is Robertsonian and hybrids have intermediate chromosome numbers) and samples were classified (on the basis of published data) according to karyotype. Group 1 consisted of samples from three English Channel populations of higher chromosome number (on average 2n > 32) and Group 2 consisted of the remaining 21 samples (presumed to be 2n= 26). Karyotype variation accounts for roughly the same amount of the absolute allozyme variance as geographic variation (46.3 °, and 53.7°, respectively). Yet the patterns of differentiation seen between karyotypes and with geographic separation are very different. In samples classified as 2n= 26 (Group 2), while there is a significant amount of heterogeneity (F_ST per locus averaged 0.128 for 10 polymorphic loci), allozyme variation occurs independently at different loci so mean genetic identity (Nei) is high: 0.972. There is only a slight decline in genetic identity with distance (genetic identity averaged 0.965 for amphi-atlantic comparisons) indicating that passive transport of juveniles or adults may contribute significantly to gene flow. Conversely, allozyme variation between karyotypes was concordant. High chromosome number populations possessed a suite of alleles at four allozyme loci (Esl-3, Lap-2, Mdh-1 and Pep-2) which were absent or rare in Group 2 samples resulting in high F_ST values for these loci (from 0.294 to 0.472) when karyotypic classes were combined. Consequently the mean genetic identity between these Robertsonian races is low, 0.856, and falls within the range more usually associated with congeneric comparisons than with con-specific comparisons. The mechanisms maintaining this genie difference are unclear. However the distribution of the karyotypes and physiological and morphological differences (in shell shape) between them strongly suggest that karyotypic variation in Nucella is adaptive.     

Microgeographic variation in allozyme frequencies in relation to the degree of exposure to wave action in the dogwhelk Nucella lapillus (L.) (Prosobranchia: Muricacea)

Nucella lapillus from 15 sites 50 m to 21 km apart in S. Devon, S. W. England were analysed for allozyme variation at eight soluble enzyme loci. Sites were classified as either Exposed or Sheltered and a hierarchical analysis of allozyme variation carried out using Wright's Fixation Index, F_ST. Whelks from Sheltered sites segregated for alleles at the Est-3, Lap-2, Pep-2 and Mdh-1 loci which were virtually absent from exposed sites resulting in high F_ST values (0.289–0.506) when all samples were included. Consequently mean heterozygosity of the Sheltered samples was roughly twice that of the Exposed. Between Sheltered sites the frequencies of these 'additional' alleles varied substantially, even on a microgeographic scale and were found to be highly correlated with exposure. Within individuals the presence of the 'sheltered' alleles was correlated with the possession of the 'sheltered' shell shape as indicated by length divided by aperture height. This must necessarily be the case, however, if both are related independently to exposure. Although these correlations imply the action of selection there is evidence within the data for stochastic factors affecting the pattern observed. Complicating the picture further is the correspondence observed in the distribution of the 'sheltered' alleles with the known distribution of chromosomal translocations. Phenotypic associations within individuals also support the hypothesis that variation at the Est-3, Lap-2, Mdh-1 and Pet-2 loci is related to variation in chromosome number. However, the nature of the relations of karyotype and allozyme variation with shell shape and exposure remain speculative.     

Cloning and primary structure of putative cytosolic and mitochondrial malate dehydrogenase from the mollusc Nucella lapillus (L.)

The evolutionary history of the malate dehydrogenase (MDH) gene family [NAD-dependent MDH; EC 1.1.1.37 and NAD(P)-dependent MDH; EC 1.1.1.82] has received much attention. MDHs have also featured extensively as electrophoretic markers in population genetics and evolutionary ecology, and in many cases, intraspecific variation in MDH has been correlated with environmental variables. However, while the amino acid residues essential for MDH function are known, no studies have examined intraspecific nucleotide variation despite evidence indicating that natural selection may be operating on this locus. This study presents two sets of degenerate oligonucleotide PCR primers to facilitate the cloning of cytosolic MDH (cMDH) and mitochondrial MDH (mMDH) from a broad range of animals (cMDH) and animals and plants (mMDH). These primers were used to obtain putative cMDH and mMDH cDNAs from the mollusc Nucella lapillus. The N. lapillus cMDH cDNA was found to encode a putative cMDH protein of 334aa and 36kDa, while the mMDH cDNA encoded a putative mature mMDH protein of 315aa and 33kDa. The putative amino acid sequences of the two compartmentalised N. lapillus MDHs are presented and compared to other known MDH sequences.     

Intersex and Littorina littorea in Cork Harbour: results of a medium-term monitoring programme

Cork Harbour, located on the south coast of Ireland, is a complex, multi-user environment. In the present study Littorina littorea (L.) is used as a bio-indicator of TBT pollution, as it has a wide range within the harbour, unlike the more common bio-indicator, Nucella lapillus (L.), which is limited to rocky substrata near the mouth of the harbour. Intersex in L. littorea is used for the first time in Ireland as a medium-term indicator of TBT pollution and results show that there are no deviations in levels of intersex over the three year period from 1994–1996. These results are discussed.     

Chromosomal polymorphism in the Atlantic dog-whelk, Nucella lapillus (Gastropoda: Muricidae): nomenclature, variation and biogeography

Nucella lapillus appears to be unique within the Muricidae, and indeed the Mollusca, in exhibiting a Robertsonian chromosomal polymorphism. The recorded diploid values range from 2 n  = 26 to 2 n  = 36, putatively brought about by fusion of smaller chromosomes to form five pairs of large metacentrics in the 2 n  = 26 form. In this study, the karyotypes of the numerically extreme forms (2 n  = 26 and 2 n  = 36) have been illustrated and described in detail, and a new scheme of nomenclature is proposed for the chromosomal rearrangements observed in N. lapillus . Chromosome numbers and karyotypes were recorded and analysed from 70 sites throughout its wide geographical range, mainly from around the UK coasts but also from sites in Norway, France, Spain, Portugal and the USA, showing remarkable variation in both diploid number and karyotypic configuration. The results provide new evidence that seven chromosomes in the 2 n  = 26 form can be involved in the Robertsonian rearrangements, but the maximum recorded diploid number remains 2 n  = 36. Inversions were confirmed in three chromosomes and one population was found to exhibit aneuploidy. Possible explanations for the geographical trends in karyotypic variation are discussed, but despite the advances in the karyology of N. lapillus , a simple solution to this enigmatic phenomenon remains elusive.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 195–210.     

Patterns of variation in tail ornament size in birds

In recent years several different kinds of sexual selection models have been developed, and tail ornaments in birds have frequently been used as an example of a sexually selected character where the models might apply. However, very little is known about intra- and interpopulation variation in ornament size. We have studied the elongated tail ornaments in four species of whydahs Vidua , the forktailed flycatcher Tyrannus savana and the Asian paradise flycatcher Terpsiphone paradisi. Ornaments were relatively longer in males with the longest tarsi ('heterogony' with positive allometry). Also, tail lengths were remarkably variable within each geographical area, the coefficient of variation (average = 11%) being three times as high as for body size characters. Models, with female preference of ornaments bearing no relation to male viability, usually generate lines of neutral equilibria. Thus, they predict extraordinary variation in ornaments between populations. However, elongated tail ornaments did not show higher geographical variation than the body size characters, suggesting that there is no line of equilibria for these ornaments.