Variation in populations of Cepaea nemoralis (L.) in North Spain

In a survey of 105 populations of Cepaea nemoralis sampled in North Spain, the distribution of morph polymorphism seems to have a climatic component. The area sampled corresponds with the two main climatic regions in the Iberian Peninsula: Green and Brown Iberia, which have an Atlantic and Continental climate, respectively. Paler colour and banding phenotypes are found in the Atlantic zone, while the dark ones are commoner in Brown Iberia. This may arise from climatic selection related to behaviour patterns, which may be particularly important in limiting situations with harsh climates.     

Variation in body colour in western Irish populations of Cepaea nemoralis (L.)

Samples of Cepaea nemoralis (L.) taken from sand-dune, lowland and mountain populations show differences in body colour. Overall, sand-dune populations are much paler than those in the other two areas. On sand-dunes, darker and more variable populations are found in densely vegetated habitats; in the lowland, darker forms occur further inland but there is no correlation with vegetation; mountain populations are darker and less variable on north- than south-facing slopes. Overall differences between areas can be ascribed to climatic selection and differences in variation within areas to niche width.     

Food overlap in co-existing populations of the land snails Cepaea nemoralis (L.) and Cepaeahortensis (Müll)

Faecal analysis of adult Cepaea nemoralis and Cepaea hortensis from a mixed population on chalk grassland shows that the two snail species select the same plant material as food. Herbs are selected in preference to grasses and Urtica dioica is particularly favoured. C. hortensis has the more pronounced preference for senescent material. These results are discussed in relation to competition between the two species.     

Pathogen resistance and genetic variation at MHC loci

Abstract.— Balancing selection in the form of heterozygote advantage, frequency-dependent selection, or selection that varies in time and/or space, has been proposed to explain the high variation at major histocompatibility complex (MHC) genes. Here the effect of variation of the presence and absence of pathogens over time on genetic variation at multiallelic loci is examined. In the basic model, resistance to each pathogen is conferred by a given allele, and this allele is assumed to be dominant. Given that s is the selective disadvantage for homozygotes (and heterozygotes) without the resistance allele and the proportion of generations, which a pathogen is present, is e , fitnesses for homozygotes become (1 — s )^(n-1)e and the fitnesses for heterozygotes become (1 — s )^(n-2)e, where n is the number of alleles. In this situation, the conditions for a stable, multiallelic polymorphism are met even though there is no intrinsic heterozygote advantage. The distribution of allele frequencies and consequently heterozygosity are a function of the autocorrelation of the presence of the pathogen in subsequent generations. When there is a positive autocorrelation over generations, the observed heterozygosity is reduced. In addition, the effects of lower levels of selection and dominance and the influence of genetic drift were examined. These effects were compared to the observed heterozygosity for two MHC genes in several South American Indian samples. Overall, resistance conferred by specific alleles to temporally variable pathogens may contribute to the observed polymorphism at MHC genes and other similar host defense loci.     

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.     

Shell polymorphism in a southern peripheral population of Cepaea nemoralis (L.) (Pulmonata: Helicidae) in Spain

Populations of the land snail Cepaea nemoralis have been investigated at the southern limits of its range in Spain, the Upper Tajo region, in order to analyse the distribution of the species and the variation of polymorphism in relation to environmental conditions. For this purpose two natural subareas, which differ in topography, soil nature, climate and vegetation have been considered. Cepaea nemoralis is confined to the river banks of the area; it is found in open and shaded biotopes of subarea 1 where it is relatively common, and it is almost restricted to shaded biotopes of subarea 2 where it becomes progressively rarer towards the south. Relative abundance of the species may be related to the amount of calcareous soils and climate, the restriction in its southern distribution being probably the result of extreme solar radiation, high temperature and low humidity. The two subareas differ in the frequency of the main polymorphic characters. These differences may be related to the kind of biotope. Subarea 1 richer in more open and exposed biotopes have higher frequencies of yellow, 00000, 00300, and unfused bands, whereas the restriction to poplar groves because of the lack of suitable exposed biotopes in subarea 2 may account for the higher proportion of pink five-bandeds with the bands fused together. This kind of variation with biotope is consistent with an explanation in terms of differences in the temperature absorbance of different morphs and a metabolic response to differences in temperature amplitude of the biotopes. Other characters (lip colour, punctate bands, hyalozonate bands, etc.) are not polymorphic in this region, thus, suggesting that at the periphery environmental conditions are important not only in determining the distribution of the species but exerting a marked effect on the genetic structure of the populations.     

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.     

Overdominance in the human genome and olfactory receptor activity

We investigate the contribution of overdominance to the maintenanceof polymorphism in the human genome during the recent evolutionof our species. Using the HapMap genotypic information, we havedetected that the Gene Ontology term "olfactory receptor activity"is a molecular function overrepresented in genes that have SNPs(Single Nucleotide Polymorphisms) showing higher than expectednumber of heterozygotes in the HapMap populations. Our resultssuggest that the diversity of a subset of human olfactory receptors(ORs) may have been maintained by balancing selection, in theform of overdominance. This observation may suggest that theloss of OR genes during the evolution of the human lineage mayhave been accompanied by an increased capability to discriminateodorants with closely similar structures.     

On the correlation between heterozygosity and fitness in natural populations

Three primary hypotheses currently prevail for correlations between heterozygosity at a set of molecular markers and fitness in natural populations. First, multilocus heterozygosity-fitness correlations might result from selection acting directly on the scored loci, such as at particular allozyme loci. Second, significant levels of linkage disequilibrium, as in recently bottlenecked-and-expanded populations, might cause associations between the markers and fitness loci in the local chromosomal vicinity. Third, in partially inbred populations, heterozygosity at the markers might reflect variation in the inbreeding coefficient and might associate with fitness as a result of effects of homozygosity at genome-wide distributed loci. Despite years of research, the relative importance of these hypotheses remains unclear. The screening of heterozygosity at polymorphic DNA markers offers an opportunity to resolve this issue, and relevant empirical studies have now emerged. We provide an account of the recent progress on the subject, and give suggestions on how to distinguish between the three hypotheses in future studies.     

MHC heterozygosity and survival in red junglefowl

Genes of the major histocompatibility complex (MHC) form a vital part of the vertebrate immune system and play a major role in pathogen resistance. The extremely high levels of polymorphism observed at the MHC are hypothesised to be driven by pathogen‐mediated selection. Although the exact nature of selection remains unclear, three main hypotheses have been put forward; heterozygote advantage, negative frequency‐dependence and fluctuating selection. Here, we report the effects of MHC genotype on survival in a cohort of semi‐natural red junglefowl (Gallus gallus) that suffered severe mortality as a result of an outbreak of the disease coccidiosis. The cohort was followed from hatching until 250 days of age, approximately the age of sexual maturity in this species, during which time over 80% of the birds died. We show that on average birds with MHC heterozygote genotypes survived infection longer than homozygotes and that this effect was independent of genome‐wide heterozygosity, estimated across microsatellite loci. This MHC effect appeared to be caused by a single susceptible haplotype (CD_c) the effect of which was masked in all heterozygote genotypes by other dominant haplotypes. The CD_c homozygous genotype had lower survival than all other genotypes, but CD_c heterozygous genotypes had survival probabilities equal to the most resistant homozygote genotype. Importantly, no heterozygotes conferred greater resistance than the most resistant homozygote genotype, indicating that the observed survival advantage of MHC heterozygotes was the product of dominant, rather than overdominant processes. This pattern and effect of MHC diversity in our population could reflect the processes ongoing in similarly small, fragmented natural populations.     

Genotypic selection in Daphnia populations consisting of inbred sibships

The genetic basis of fitness reduction associated with inbreeding is still poorly understood. Here we use associations between allozyme genotypes and fitness to investigate the genetic basis of inbreeding depression in experimental outdoor populations of the water flea, Daphnia magna. In Daphnia, a phase of clonal reproduction follows hatching from sexually produced resting eggs, and changes in genotype frequencies during the clonal phase can be used to estimate fitness. Our experiment resembles natural colonization of ponds in that single clones colonize an empty pool, expand asexually and produce sexual offspring by selfing (sisters mate with their clonal brothers). These offspring diapause and form populations consisting of selfed sibships in the following spring. In 12 of 13 experimental populations, genotypes of selfed hatchlings after diapause conformed to Mendelian expectations. During the subsequent ca. 10 asexual generations, however, genotype frequencies changed significantly at 19 of 27 single loci studied within populations, mostly in favour of heterozygotes, with heterozygosity at multiple loci affecting the change in genotype frequency multiplicatively. Because variance in heterozygosity among siblings at a given marker reflects only heterozygosity in the chromosomal region around this marker, our results suggest that selection at fitness-associated loci in the chromosomal regions near the markers were responsible for these changes. The genotype frequency changes were more consistent with selection acting on linked loci than on the allozymes themselves. Taken together, the evidence for abundant selection in the chromosomal regions of the markers and the fact that changes in genotype frequencies became apparent only after several generations of clonal selection, point to a genetic load consisting of many alleles of small or intermediate effects, which is consistent with the strong genetic differentiation and repeated genetic bottlenecks in the metapopulation from which the animals for this study were obtained.     

The evolution of the major histocompatibility complex in upstream versus downstream river populations of the longnose dace

Populations in upstream versus downstream river locations can be exposed to vastly different environmental and ecological conditions and can thus harbor different genetic resources due to selection and neutral processes. An interesting question is how upstream–downstream directionality in rivers affects the evolution of immune response genes. We used next‐generation amplicon sequencing to identify eight alleles of the major histocompatibility complex (MHC) class II β exon 2 in the cyprinid longnose dace (Rhinichthys cataractae) from three rivers in Alberta, upstream and downstream of municipal and agricultural areas along contaminant gradients. We used these data to test for directional and balancing selection on the MHC. We also genotyped microsatellite loci to examine neutral population processes in this system. We found evidence for balancing selection on the MHC in the form of increased nonsynonymous variation relative to neutral expectations, and selection occurred at more amino acid residues upstream than downstream in two rivers. We found this pattern despite no population structure or isolation by distance, based on microsatellite data, at these sites. Overall, our results suggest that MHC evolution is driven by upstream–downstream directionality in fish inhabiting this system.     

Signals of major histocompatibility complex overdominance in a wild salmonid population

The major histocompatibility complex (MHC) contains the most variable genes in vertebrates, but despite extensive research, the mechanisms maintaining this polymorphism are still unresolved. One hypothesis is that MHC polymorphism is a result of balancing selection operating by overdominance, but convincing evidence for overdominant selection in natural populations has been lacking. We present strong evidence consistent with MHC-specific overdominance in a free-living population of Arctic charr (Salvelinus alpinus) in northernmost Europe. In this population, where just two MHC alleles were observed, MHC heterozygous fish had a lower parasite load, were in better condition (as estimated by a fatness indicator) and had higher survival under stress than either of the homozygotes. Conversely, there was no consistent association between these fitness measures and assumedly neutral microsatellite variability, indicating an MHC-specific effect. Our results provide convincing empirical evidence consistent with the notion that overdominance can be an important evolutionary mechanism contributing to MHC polymorphism in wild animal populations. They also support a recent simulation study indicating that the number of alleles expected to be maintained at an MHC loci can be low, even under strong heterozygote advantage.     

Wild birds prefer the familiar morph when feeding on pastry-filled shells of the landsnail Cepaea hortensis (Müll.)

Colour polymorphisms in prey could be maintained if predators concentrate on common morphs and confer a selective advantage on rare morphs. We describe experiments to test whether wild birds feed on pastry-stuffed shells of Cepaea hortensis in a manner that might lead to such apostatic selection. The birds were first given a 'pre-training' choice test of a shell population with equal numbers of yellow unbandeds and yellow five-bandeds; they were then trained on one morph alone, given a second choice test, trained on the other morph and, finally, given a third choice test. The birds preferred five-bandeds in five of the six pre-training tests. In all six experiments the first training session increased the birds' preferences for the morph that was familiar. The results were less clear-cut when selection during pre-training was compared with selection after the second training session. However, a comparison between selection after each of the two training sessions showed that in all six experiments the results were in the direction predicted from the hypothesis that familiar morphs are preferred. This set of experiments is one of the few in which behaviour which could lead to apostatic selection has been tested with morphs that differ in pattern. The findings support the idea that polymorphism in Cepaea could be maintained by apostatic selection.     

Allelic divergence precedes and promotes gene duplication

One of the striking observations from recent whole-genome comparisons is that changes in the number of specialized genes in existing gene families, as opposed to novel taxon-specific gene families, are responsible for the majority of the difference in genome composition between major taxa. Previous models of duplicate gene evolution focused primarily on the role that neutral processes can play in evolutionary divergence after the duplicates are already fixed in the population. By instead including the entire cycle of duplication and divergence, we show that specialized functions are most likely to evolve through strong selection acting on segregating alleles at a single locus, even before the duplicate arises. We show that the fitness relationships that allow divergent alleles to evolve at a single locus largely overlap with the conditions that allow divergence of previously duplicated genes. Thus, a solution to the paradox of the origin of organismal complexity via the expansion of gene families exists in the form of the deterministic spread of novel duplicates via natural selection.     

Heterosis, epistasis and linkage disequilibrium in a wild population of the polymorphic butterfly Danaus chrysippus (L.)

The colour polymorphism of the Danaus chrysippus population at Dar es Salaam, East Africa, is controlled at three major loci, each with two alleles. Two of the loci, one governing ground colour and the other forewing pattern, are closely linked. The third locus, determining hindwing pattern, assorts independently. Thirty-eight broods raised from wild mated pairs, Fl and F2 generations gave 857 offspring of 23 genotypes (out of 27 possible). The forewing length, taken as an index of size, was investigated in relation to the genotype. Heterosis is evident at all three loci. The two linked loci show epistatic interaction of an unexpected kind: double heterozygotes are smaller than heterozygotes at only one locus but larger than double homozygotes. The heterotic effect at the third, unlinked locus is the most pronounced and is additive to that at the other two. Heterosis is more marked in males than females. The possibility that body size has importance in connexion with sexual selection, food resources and mimetic relationships is discussed. Analysis of gene and chromosome frequencies in the wild parents of 61 broods suggests that double heterozygotes for the two linked loci may have heterozygous advantage. Seventy-eight per cent of chromosomes are repulsion phase: thus, there is pronounced linkage disequilibrium which must be maintained by selection as crossing over is almost 296. In particular, the chromosome carrying both dominant alleles in coupling is rare. Consideration of the centres of distribution and present ranges of the alleles at all three loci suggests that three geographical races, aegyptius, dorippus and alcippus, were isolated by forest barriers, during wet periods in the Pleistocene, in south-west, north-east and north-west Africa respectively. They have probably expanded their ranges in the post-glacial period to overlap and interbreed in central and east Africa. Either heterozygous advantage or seasonal (directional) selection or a combination of both is responsible for the persistence of the polymorphism.     

Growth rate correlates to individual heterozygosity in the European eel, Anguilla anguilla L

Heterozygosity-fitness correlations (HFCs) have been reported in populations of many species. We provide evidence for a positive correlation between genetic variability and growth rate at 12 allozyme loci in a catadromous marine fish species, the European eel (Anguilla anguilla L.). More heterozygous individuals show a significantly higher length and weight increase and an above average condition index in comparison with more homozygous individuals. To a lesser extent, six microsatellite loci show a similar pattern, with positive but not significant correlations between heterozygosity and growth rate. The HFCs observed could be explained by an effect of either direct allozyme over-dominance or associative overdominance. Selection affecting some of the allozyme loci would explain the greater strength of the HFCs found at allozymes in comparison with microsatellites and the lack of correlation between MLH at allozymes and MLH at microsatellites. Associative overdominance (where allozyme loci are merely acting as neutral markers of closely linked fitness loci) might provide an explanation for the HFCs if we consider that allozyme loci have a higher chance than microsatellites to be in linkage disequilibrium with fitness loci.     

Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris)

The fundamental role of the major histocompatibility complex (MHC) in immune recognition has led to a general consensus that the characteristically high levels of functional polymorphism at MHC genes is maintained by balancing selection operating through host–parasite coevolution. However, the actual mechanism by which selection operates is unclear. Two hypotheses have been proposed: overdominance (or heterozygote superiority) and negative frequency-dependent selection. Evidence for these hypotheses was evaluated by examining MHC–parasite relationships in an island population of water voles (Arvicola terrestris). Generalized linear mixed models were used to examine whether individual variation at an MHC class II DRB locus explained variation in the individual burdens of five different parasites. MHC genotype explained a significant amount of variation in the burden of gamasid mites, fleas (Megabothris walkeri) and nymphs of sheep ticks (Ixodes ricinus). Additionally, MHC heterozygotes were simultaneously co-infected by fewer parasite types than homozygotes. In each case where an MHC-dependent effect on parasite burden was resolved, the heterozygote genotype was associated with fewer parasites, and the heterozygote outperformed each homozygote in two of three cases, suggesting an overall superiority against parasitism for MHC heterozygote genotypes. This is the first demonstration of MHC heterozygote superiority against multiple parasites in a natural population, a mechanism that could help maintain high levels of functional MHC genetic diversity in natural populations.     

Maladaptive mate choice maintained by heterozygote advantage

Common buzzards (Buteo buteo) show a plumage polymorphism that appears to be maintained by heterozygote advantage and allows a maladaptive form of mate choice to persist. The light and dark morphs have a much lower fitness than the presumed heterozygous intermediate morph, but are replenished through Mendelian segregation in intermediate-intermediate pairs. Light and dark morphs could maximize their fitness by mating light with dark to produce all intermediate offspring, but instead choose partners of their own color, thereby producing broods of minimally fit homozygotes. Such maladaptive behavior argues forcefully against mate choice based on "good genes," and its persistence is best explained by heterozygote advantage maintaining the polymorphism coupled with nongenetic mate choice based on sexual imprinting. Modeling different patterns of mate choice shows that random mating and preference for own morph fit our data poorly, whereas preference for mother's morph yields a good fit.