Seasonal variation of microhabitat distribution of the polymorphic land snail Cepaea nemoralis

We studied the seasonal variation of microhabitat distribution of the land snail Cepaea nemoralis over a 3-year period in a population at Dansville, New York. Stratified random quadrat sampling was used to determine snail densities and environmental variables in each month. The plant cover of each quadrat was estimated by a modified Daubenmire measure. Canonical correlation analysis was used to investigate the relationship between the morph density and the environmental variables. Significant relations existed between snail morphs and environmental variables in 8 of the 13 months analyzed. Temperature and rainfall are two important factors affecting such relations. In hot and dry summer months, morphs had a stronger canonical correlation with the environmental variables than in cool and wet months. Food and shelter were important in determining distribution over habitats of the snail. Food was primarily responsible for snail distribution over habitats in the early summer. As the weather became hot and dry, the importance of shelter became more evident. Both banded and unbanded morphs tended to be associated strongly with sheltered microhabitats in hot dry seasons.     

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.     

Patterns of morphological and molecular polymorphism in the land snail Cepaea nemoralis

In the land snail Cepaea nemoralis , allele frequencies at loci controlling shell polymorphisms often show large areas of remarkable constancy which are separated by steep clines from neighbouring areas with strikingly different allele frequencies. It has recently been claimed that these 'area effects' exemplify a general tendency for population differentiation without geographic isolation in a variety of organisms of relatively low mobility. As such they could represent an early phase in the process of speciation. If this is true, population differentiation of shell polymorphisms in Cepaea would be expected to be accompanied by parallel differentiation at other gene loci, such as those detected by gel electrophoresis.
We have studied populations of C. nemoralis in North Wales and in the Valle de Aran of the Pyrenees. Levels of molecular heterogeneity are comparable to those found in related animals which show much less visible polymorphism. In spite of some statistical problems inherent in the analysis ol overlapping geographic patterns, there is no clear association between the patterns of geographic variation at the visible and molecular levels. Claims that genetic differentiation in the visible polymorphisms between C. nemoralis populations are a special case of the formation of geographic races are therefore probably not justified.     

Certain mathematical models to describe the dynamics of polymorphic populations of the land snail Cepaea nemoralis (L.)

Wolda has produced a model to describe the dynamics of monomorphic populations of Cepaea nemoralis. This paper indicates how the model can be extended to incorporate the much studied shell pattern polymorphisms of the species, and suggests some simplifications which may be of value.     

Food,feeding rates and assimilation in the land snail Cepaea nemoralis L.

Summary The natural diet of a population of Cepaea nemoralis living in a sand dune system in southwest England was investigated by field observations and examination of crop and faeces contents. The food consisted of dead material from the commoner plants on the site. Very little green matter was eaten and there was little evidence for seasonal variation in the diet.Consumption and egestion rates were measured gravimetrically on natural foods (dead leaves of Taraxacum officinale and Ononis repens) and artificial foods. Consumption rates were temperature dependent over the measured range of 5–20°C and also varied with the food substrate, an artificial food (rat food pellets) being consumed at the highest rate. High variability in the results can probably be linked to the live weight and activity cycles of the snails.Assimilation was estimated as the difference between consumption and egestion, since a trial of the ash-ratio method proved unsuitable with this animal. Assimilation efficiency did not vary with temperature over the range studied, but was dependent on food substrate, the two artificial foods (rat food pellets and lettuce leaves) being assimilated more efficiently (71–73%) than natural foods (30–44%).Faeces produced from the digestive gland could be distinguished and were measured separately. The amount produced was very small compared to the gut faeces, but increased significantly when a relatively indigestible food was used.     

The effect of artificial photoperiod on growth and reproduction in the land snail Cepaea nemoralis

Summary

Specimens of Cepaea nemoralis were raised from egg to adult in the laboratory for 15.5 months in two artificial photoperiods: short-day (LD 8:16) and long-day (LD 16:8). Over 20% of the snails in each photoperiod were functional adults by the end of the experiment and had fully developed male and female reproductive systems as determined both by dissection and by oviposition. A total of 925 eggs were laid by animals reared in a long-day photoperiod, whereas animals in a short-day photoperiod laid 677 eggs. Animals reared in a long-day photoperiod grew slightly faster (2.04 mg/day compared to 1.73 mg/day), began laying eggs about 18 days sooner, and suffered higher mortality (19% compared to 11%) than animals reared in a short-day photoperiod. These results clearly establish for C. nemoralis that gametogenesis and the development of a functional hermaphroditic reproductive system are neither prevented nor significantly retarded by exposing the animals to a short-day photoperiod for their entire pre-reproductive life.     

Opioid systems,behavioral thermoregulation and shell polymorphism in the land snail,Cepaea nemoralis

Summary Numerous ecological studies have dealt with the shell color and banding polymorphism of the land snail Cepaea nemoralis. The present field and laboratory investigations focus on the roles of opioid systems in modulating the thermal preferences and behavioral thermoregulation of various morphological types of Cepaea. Evidence is presented that differences in opioid modulation of the thermal responses of Cepaea are associated with shell polymorphism. It is shown that the effects of the prototypic opiate agonist, morphine, and antagonist, naloxone, on behavioral thermoregulation in Cepaea vary with the shell banding pattern and thermal microhabitat. In both the field and laboratory, morphine (0.10, 1.0 and 10 g per snail) caused significant dose- and time-dependent increases in the temperatures selected by various morphological types of Cepaea. The palest shell type (yellow, unbanded) with the highest basal preferred temperature displayed the greatest response to morphine, the shell type (yellow, 2-banded) with an intermediate basal preferred temperature showed an intermediate response to morphine, and the darkest shell type (yellow, 5-banded) with lowest basal preferred temperature showed the least increase in preferred temperature after administration of morphine. These effects of morphine were blocked and reversed by naloxone (1.0 g), with the opiate antagonist by itself (1.0 and 10 g) causing a significant decrease in behaviorally selected temperatures. The unbanded and 2-banded morphs displayed significantly greater decreases in preferred temperatures after treatment with naloxone than did the 5-banded morph, which showed minimal responses. It is suggested that these differences in opioid modulation of thermal preferences and behavioral thermoregulation may contribute to the polymorphic thermal preferences of natural populations of Cepaea.Abbreviations B yellow five-banded shell type - I yellow two-banded shell type - U yellow unbanded shell type     

Rapid evolution in unstable habitats: a success story of the polymorphic land snail Cepaea nemoralis (Gastropoda: Pulmonata)

The present study reports on a natural experiment with twelve replicates in which rapid, predictable and consistent divergence of Cepaea nemoralis populations occurred in response to repeated selection gradient of adjacent open and shaded habitats. Because the frequencies of various genetically‐based phenotypes varied widely among surveyed populations, and there was a large overlap between habitat types, no overall association with habitat was apparent. In paired comparisons, however, significant changes were consistently towards higher frequencies of light morphs in the open than corresponding shaded habitats, and this result is attributable to natural selection. This shows that the knowledge of the genetic composition of reference populations is often essential for discerning selection from random processes. At each site, a different morph combination contributed to the divergence of populations, indicating that there are many genetic solutions to similar ecological problems; this likely enhances the maintenance of high levels of polymorphism. Adaptation of populations occurred in contemporary time and was fast. In one case where it was possible to follow changes, significant shifts in morph frequencies occurred within just two snail generations (selection coefficients of 0.404 and 0.518). High evolvability may be one of the factors contributing to the ecological success of Cepaea nemoralis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 251–262.     

Fate of dietary linoleic and linolenic acids in the land snail Cepaea nemoralis (L.)

• 1.1. Linoleic and linolenic acids resorbed from the diet are introduced into the lipid metabolism, but a major part is degradated to carbon dioxide, negating any obvious sparing effect.
• 2.2. Despite the predominance of the linoleic fatty acid series in the snail structural lipids linoleic acid is less effectively incorporated into the phospholipids than is linolenic acid, which may be correlated with the de novo production of linoleic acid in the snail.
• 3.3. Linoleic and linolenic acid chains incorporated into the phospholipids are rapidly elongated and dehydrogenated, while in the triglycerides these precursor acids remain metabolically unaltered.

     

Spatial genetic structure in a metapopulation of the land snail Cepaea nemoralis (Gastropoda: Helicidae)

Habitat fragmentation is a major force affecting demography and genetic structure of wild populations, especially in agricultural landscapes. The land snail Cepaea nemoralis (L.) was selected to investigate the impact of habitat fragmentation on the spatial genetic structure of an organism with limited dispersal ability. Genetic and morphological patterns were investigated at a local scale of a 500 m transect and a mesoscale of 4 x 4 km in a fragmented agricultural landscape while accounting for variation in the landscape using least-cost models. Analysis of microsatellite loci using expected heterozygosity (HE), pairwise genetic distance (FST/1-FST) and spatial autocorrelograms (Moran's I) as well as shell characteristics revealed spatial structuring at both scales and provided evidence for a metapopulation structure. Genetic diversity was related to morphological diversity regardless of landscape properties. This pointed to bottlenecks caused by founder effects after (re)colonization. Our study suggests that metapopulation structure depended on both landscape features and the shape of the dispersal function. A range of genetic spatial autocorrelation up to 80 m at the local scale and up to 800 m at the mesoscale indicated leptokurtic dispersal patterns. The metapopulation dynamics of C. nemoralis resulted in a patchwork of interconnected, spatially structured subpopulations. They were shaped by gene flow which was affected by landscape features, the dispersal function and an increasing role of genetic drift with distance.     

The habitats of the land snail Cepaea nemoralis (L.) on downland and their ecogenetie significance

Population densities of adult Cepaea nemoralis (L.) were estimated for nine chalk grassland sites on the South Downs. Estimates of cover, species composition and height of vegetation were also obtained. The density of C. nemoralis was positively associated with Bromus erectus cover, and negatively with Festuca spp. cover. This finding, confirmed by an earlier survey, suggests that the density of C. nemoralis in chalk grassland is directly or indirectly governed by mammalian grazing pressure, and not by the availability of suitable food. Intensely grazed downland is an unsuitable, or at best a marginal habitat for C. nemoralis. This conclusion is discussed with particular reference to 'area effects' in the shell character polymorphism, often found in downland populations of C. nemoralis.     

Morph frequencies in the snail Cepaea nemoralis: changes with time and their interpretation

Colonies of the polymorphic snail Cepaea nemoralis on the sand dune at Point of Air, north Wales, first sampled in 1962 by A.J. Cain and P.M. Sheppard, have been re-sampled after 35 years. The frequency of the mid-banded morph has increased. Overall, yellow frequency has decreased at the expense of pink, but the change is in different directions in different parts of the dune. Yellow mid-banded and pink five-banded, phenotype combinations controlled by alleles at unlinked loci, are in excess within colonies, which suggests an effect of selection. It is argued that changes in morph frequency are due, at least in part, to movement between colonies. Cepaea populations are slow to respond to environmental changes and displacement of individuals may be greater than is often assumed. It is therefore difficult to interpret frequency changes over time. Correlated changes in groups of colonies may not always be interpretable as indicating selection.     

Colonization,stability, and adaptation in a transplant experiment of the polymorphic land snail Cepaea nemoralis (Gastropoda: Pulmonata) at the edge of its geographical range

At the eastern margins of the geographical distribution in Europe, populations of Cepaea nemoralis are sparse and limited to urban environments to which they are possibly confined by relatively warmer climates. In 1999 we introduced 1101 C. nemoralis individuals originating from nine urban populations to a rural location in the area. The snails established a viable population, which suggests that confinement to urban settings is dispersal‐ rather than climate‐limited. The snails filled available habitats at a rate of approximately 400–600 m² year^?1. On the whole, morph frequencies remained remarkably stable; changes that occurred are attributable to segregation of alleles or chromosomes. However, snails responded to habitat heterogeneity: consistent and predictable divergence occurred between habitat types, such that light‐shelled snails were repeatedly more frequent in the open than in adjoining shaded habitats. This suggests the operation of climatic and/or visual selection. As the whole area encompassing seven distinct habitat patches was only 0.3 ha, and the maximum duration of population divergence was only 11 years (fewer than four snail generations), these results indicate extremely small temporal and spatial scales of adaptation during initial phases of population establishment and spread. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 462–470.     

Geographic structuring of molecular and morphological polymorphism in Pyrenean populations of the snail Cepaea nemoralis

To determine whether geographic patterns of variation in the frequency of shell polymorphisms in the land snail Cepaea nemoralis mark regions of extensive genetic differentiation, allele frequencies at six polymorphic enzyme-encoding loci were analyzed electrophoretically in 74 samples from the central part of the Spanish Pyrenees. Within a large area effect for unbanded shells on the southern slope of the Pyrenees, there is no enzyme locus at which allele frequencies are homogeneous. Because this morphological area effect does not mark a region of pervasive genetic change, the genetic structure of populations in the region studied does not conform to recent models of area effect speciation. Factor analysis of allele frequencies at three loci controlling shell polymorphisms and six enzyme loci separated populations on the southern slope into two groups, one of which is similar to the group of populations on the northern slope. There is therefore considerable geographic structuring of both molecular and morphological polymorphism in this species.     

Selection and disequilibrium in Cepaea nemoralis

The snail Cepaea nemoralis (L.) is usually polymorphic for linked loci conferring pink or yellow shell ground colour and banding or lack of bands. An unlinked locus, mid‐banded, modifies the appearance of banded shells. These characters have a very wide range of frequencies across the species range and even within limited areas. In Britain, frequencies differ between populations from shaded woodland habitats and those from closely adjacent open habitats. Using data from the Evolution MegaLab Project, it is shown that the greater frequency of pink unbanded in shaded habitats is associated with a greater excess of the favoured allele combinations, measured as linkage disequilibrium. Examination of the relationship of disequilibrium to allele frequency in samples from the full geographical range and all habitats and climates shows that, in general, the allele combinations at high frequencies are in gametic excess. This suggests that selection tends to diversify rather than move frequencies towards stable equilibria. The result is important in relation to the as yet unresolved question how the polymorphism is maintained. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.