Sexual selection maintains whole-body chiral dimorphism in snails

Although the vast majority of higher animals are fixed for one chiral morph or another, the cause for this directionality is known in only a few cases. In snails, for example, rare individuals of the opposite coil are unable to mate with individuals of normal coil, so directionality is maintained by frequency-dependent selection. The snail subgenus Amphidromus presents an unexplained exception, because dextral (D) and sinistral (S) individuals occur sympatrically in roughly equal proportions (so-called 'antisymmetry') in most species. Here we show that in Amphidromus there is sexual selection for dimorphism, rather than selection for monomorphism. We found that matings between D and S individuals occur more frequently than expected by chance. Anatomical investigations showed that the chirality of the spermatophore and the female reproductive tract probably allow a greater fecundity in such inter-chiral matings. Computer simulation confirms that under these circumstances, sustained dimorphism is the expected outcome.     

Evolution of whole-body enantiomorphy in the tree snail genus Amphidromus

Diverse animals exhibit left-right asymmetry in development. However, no example of dimorphism for the left-right polarity of development (whole-body enantiomorphy) is known to persist within natural populations. In snails, whole-body enantiomorphs have repeatedly evolved as separate species. Within populations, however, snails are not expected to exhibit enantiomorphy, because of selection against the less common morph resulting from mating disadvantage. Here we present a unique example of evolutionarily stable whole-body enantiomorphy in snails. Our molecular phylogeny of South-east Asian tree snails in the genus Amphidromus indicates that enantiomorphy has likely persisted as the ancestral state over a million generations. Enantiomorphs have continuously coexisted in every population surveyed spanning a period of 10 years. Our results indicate that whole-body enantiomorphy is maintained within populations opposing the rule of directional asymmetry in animals. This study implicates the need for explicit approaches to disclosure of a maintenance mechanism and conservation of the genus.     

Postradiation changes in the brain asymmetry and higher mental functions of right- and left-handed subjects (the sequelae of the accident at the Chernobyl Atomic Electric Power Station)

The present study was aimed at comparative electrophysiological, clinical, and neurophysiological assessment of the brain functional state in dextrals (50 men) and sinistrals (5 men), who participated in the Chernobyl clean. The patients were observed over the course of 10 years (from 1990 to 1999). The results of examination of healthy persons (20 dextrals and 10 sinistrals) were used as a control. The clinical examination revealed the earlier manifestation and more severe development of paroxysmal and epileptic seizures in sinistrals than in dextrals. Electrophysiological study showed a progressive decrease in interhemispheric asymmetry of the EEG coherence characteristic for a healthy brain to inversion of its sign. These changes were more pronounced in sinistrals. In the remote terms after radiation, the interhemispheric EEG coherence decreased over the whole cortex, especially, in the frontal and central areas in both groups of patients. Neurophysiological study revealed a progressive impairment of voluntary motor activity and tactile sensibility, especially, in the left hand. These defects were more expressed in sinistrals than in dextrals. The results of complex and longitudinal examination suggest that the observed changes in brain asymmetry and interhemispheric interaction can be not only a result of a dysfunction of subcortical limbic-reticular and mediobasal brain structures but also a result of the white matter damage including corpus callosum. More expressed impairments in sinistrals than in dextrals can be explained by specific morphofunctional organization of the brain in persons with different sensor and motor asymmetries.     

Familial Sinistrals Avoid Exact Numbers

We report data from an internet questionnaire of sixty number trivia. Participants were asked for the number of cups in their house, the number of cities they know and 58 other quantities. We compare the answers of familial sinistrals – individuals who are left-handed themselves or have a left-handed close blood-relative – with those of pure familial dextrals – right-handed individuals who reported only having right-handed close blood-relatives. We show that familial sinistrals use rounder numbers than pure familial dextrals in the survey responses. Round numbers in the decimal system are those that are multiples of powers of 10 or of half or a quarter of a power of 10. Roundness is a gradient concept, e.g. 100 is rounder than 50 or 200. We show that very round number like 100 and 1000 are used with 25% greater likelihood by familial sinistrals than by pure familial dextrals, while pure familial dextrals are more likely to use less round numbers such as 25, 60, and 200. We then use Sigurd’s (1988, Language in Society) index of the roundness of a number and report that familial sinistrals’ responses are significantly rounder on average than those of pure familial dextrals. To explain the difference, we propose that the cognitive effort of using exact numbers is greater for the familial sinistral group because their language and number systems tend to be more distributed over both hemispheres of the brain. Our data support the view that exact and approximate quantities are processed by two separate cognitive systems. Specifically, our behavioral data corroborates the view that the evolutionarily older, approximate number system is present in both hemispheres of the brain, while the exact number system tends to be localized in only one hemisphere.     

Opposite shell-coiling morphs of the tropical land snail Amphidromus martensi show no spatial-scale effects

Much can be learned about evolution from the identification of those factors maintaining polymorphisms in natural populations. One polymorphism that is only partially understood occurs in land snail species where individuals may coil clockwise or anti-clockwise. Theory shows that polymorphism in coiling direction should not persist yet species in several unrelated groups of land snails occur in stably polymorphic populations. A solution to this paradox may advance our understanding of evolution in general. Here, we examine two possible explanations: firstly, negative frequency-dependent selection due to predation; secondly, random fixation of alternative coiling morphs in tree-sized demes, giving the impression of wider polymorphism. We test these hypotheses by investigating morph-clustering of empty shells at two spatial scales in Amphidromus martensi populations in northern Borneo: the spatial structure of snail populations is relatively easy to estimate and this information may support one or other of the hypotheses under test. For the smaller scale we make novel use of a statistic previously used in botanical studies (the K-function statistic), which allows clustering of more than one morph to be simultaneously investigated at a range of scales and which we have corrected for anisotropy. We believe this method could be of more general use to ecologists. The results show that consistent clustering or separation of morphs cannot be clearly detected at any spatial scale and that predation is not frequency-dependent. Alternative explanations that do not require strong spatial structuring of the population may be needed, for instance ones involving a mechanism of selection actively maintaining the polymorphism.     

Enantiomorphs differ in shape in opposite directions between populations

Abstract Development is left–right reversed between dextral and sinistral morphs of snails. In sympatry, they share the same gene pool, including polygenes for shell shape. Nevertheless, their shell shapes are not the mirror images of each other. This triggered a debate between hypotheses that argue either for a developmental constraint or for zygotic pleiotropic effects of the polarity gene. We found that dextrals can be wider or narrower than sinistrals depending on the population, contrary to the prediction of invariable deviation under a developmental constraint. If the pleiotropy is solely responsible instead, the mean shape of each morph should change, depending on the frequency of polarity genotype. Our simulations of this mean shape change under zygotic pleiotropy, however, show that the direction of interchiral difference remains the same regardless of genotype frequency. Our results suggest the presence of genetic variation among populations that changes the maternal or zygotic pleiotropic effect of the polarity gene.     

Internal selection against the evolution of left-right reversal

Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood. Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistral snails that share the same zygotic genotype. Before hatching, these sinistrals developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrals. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.     

THE CONSEQUENCES OF BEING DIFFERENT: SINISTRAL COILING IN CERION

The overwhelming predominance of dextral coiling in gastropods is an outstanding and puzzling phenomenon. A few sinistral specimens (left coiling individuals) have been found in many dextral species. Only six sinistral shells have ever been found in Cerion; we base this analysis on the five available shells. We ask whether reversed symmetry is a simple either-or switch without further consequences for shell form, or whether sinistrality engenders associated effects, making left-coiling shells unlike their dextral deme-mates in other ways. All five sinistral shells differ in features of size and coiling late in growth, leading to relatively small apertures and a slight twist in the axis of coiling. We detect and measure this effect as follows: in multivariate morphospace, sinistrals occupy peripheral positions among their dextral deme-mates; in univariate analysis, sinistrals are consistently different for a set of characters involving covariance patterns never before seen in a decade of studies on ontogenetic and age-standardized variation in dextrals; a bootstrap procedure does not recover similar patterns in randomly constituted samples of dextrals matching the true sinistral distribution; direct x-ray measures of the coiling axis detect its slight twist in sinistrals. We discuss the implications of these unsuspected associations for the issues of developmental constraint upon the evolution of morphology.     

Multiple reversals of chirality in the land snail genus Albinaria (Gastropoda,Clausiliidae)

Reversed chirality has frequently evolved in snails, although the vast majority coils dextrally. However, there are often sinistral species within a dextral genus or almost exclusively sinistral families, such as the Clausiliidae. Some populations of the predominantly sinistral clausiliid genus Albinaria, in the southern Greek mainland, coil dextrally. The origin, evolution and distribution of the dextral Albinaria are puzzling, and as there is no reliable phylogenetic reconstruction for this speciose genus, it remains unclear how many times a shift in chirality has really occurred. In this study, our aim was to elucidate the evolutionary pathways of dextrality in Albinaria. We undertook a molecular phylogenetic analysis of two mtDNA (16S and COI) and one nDNA marker (ITS1) and included dextral and sinistral representatives found in syntopy or not. Both mtDNA and nDNA tree topologies imply that dextrals did not evolve as a monophyletic lineage. Instead, dextral lineages have evolved from sinistral ancestors multiple times independently. The fragmented population structure in Albinaria facilitates genetic drift and contributes to fixation of the opposite chirality and overcoming of the mating disadvantage of left–right reversal. Stochastic phenomena and biogeographical barriers have trapped those reversals in a limited geographical area.     

The effect of coil phenotypes and genotypes on the fecundity and viability of Partula suturalis and Lymnaea stagnalis: implications for the evolution of sinistral snails

Why are sinistral snails so rare? Two main hypotheses are that selection acts against the establishment of new coiling morphs, because dextral and sinistral snails have trouble mating, or else a developmental constraint prevents the establishment of sinistrals. We therefore used an isolate of the snail Lymnaea stagnalis, in which sinistrals are rare, and populations of Partula suturalis, in which sinistrals are common, as well as a mathematical model, to understand the circumstances by which new morphs evolve. The main finding is that the sinistral genotype is associated with reduced egg viability in L. stagnalis, but in P. suturalis individuals of sinistral and dextral genotype appear equally fecund, implying a lack of a constraint. As positive frequency‐dependent selection against the rare chiral morph in P. suturalis also operates over a narrow range (< 3%), the results suggest a model for chiral evolution in snails in which weak positive frequency‐dependent selection may be overcome by a negative frequency‐dependent selection, such as reproductive character displacement. In snails, there is not always a developmental constraint. As the direction of cleavage, and thus the directional asymmetry of the entire body, does not generally vary in other Spiralia (annelids, echiurans, vestimentiferans, sipunculids and nemerteans), it remains an open question as to whether this is because of a constraint and/or because most taxa do not have a conspicuous external asymmetry (like a shell) upon which selection can act.     

DIRECT AND INDIRECT ESTIMATES OF SEED VERSUS POLLEN MOVEMENT WITHIN A POPULATION OF PONDEROSA PINE

We examined the spatial distribution of maternally inherited mitochondrial DNA and paternally inherited chloroplast DNA polymorphisms in a permanently marked stand of ponderosa pine (Pinus ponderosa Laws). Movement of maternally inherited mtDNA occurs only via seed dispersal, and mtDNA haplotypes showed significant patch structure. Moreover, individuals within patches identified by mtDNA haplotypes were related approximately as half-sibs based upon analysis of allozyme genotypes. Thus, seed dispersal is limited within the population, and creates matrilineal clusters in space. By contrast, paternally inherited cpDNA is dispersed by movement of both seed and pollen. Chloroplast DNA polymorphisms showed no evidence of patch structure, but rather a weak (and nonsignificant) trend toward hyperdispersion, suggesting nearly unlimited movement of pollen among trees within this stand. Two of the trees had unique allozyme alleles, which were used to directly measure pollen movement away from those trees. Marked pollen was as likely to disperse across the population as it was to fertilize near neighbors.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Assumed and inferred spatial structure of populations: the Scandinavian brown bears revisited

We reanalysed the spatial structure of the Scandinavian brown bear (Ursus arctos) population based on multilocus genotypes. We used data from a former study that had presumed a priori a specific population subdivision based on four subpopulations. Using two independent methods (neighbour-joining trees and Bayesian assignment tests), we analysed the data without any prior presumption about the spatial structure. A subdivision of the population into three subpopulations emerged from our study. The genetic pattern of these subpopulations matched the three geographical clusters of individuals present in the population. We recommend considering the Scandinavian brown bear population as consisting of three (instead of four) subpopulations. Our results underline the importance of determining genetic structure from the data, without presupposing a structure, even when there seems to be good reason to do so.     

Genital dimorphism in natural populations of the land snail Chondrina clienta and the influence of the environment on its expression

Several species of simultaneously hermaphroditic land snails show a genital dimorphism: aphallic individuals differ from euphallic ones by a lack of male copulatory organs (penis plus genital retractor muscle). Aphallic individuals can self-fertilize or outcross as females but not as males. Thus, the mating system of a population may be significantly influenced by the proportion of aphallic individuals.
We present data on the frequency of aphally in 23 natural populations of the rock-dwelling land snail Chondrina clienta on the Baltic island of Öland, Sweden. The populations varied greatly in percentage of aphallic individuals, ranging from 52.2 to 99.1%, (grand mean 77.7%)). This variation did not follow any geographical pattern.
In a laboratory experiment, we examined whether food supply (high or low) and/or population density (high or low) experienced during ontogeny affected the expression of genital dimorphism. Snails derived from a population with 99.1% aphallic individuals and raised under different food and density conditions did not differ from the original population in frequency of aphally. By contrast, when snails from a population with 66.7% aphallic individuals were raised on a low food supply, more individuals became euphallic than expected under complete genetic determination. These results suggest that, in addition to a genetic component. the expression of the genital dimorphism can be influenced by environmental conditions.     

The influence of multiple dispersal mechanisms and landscape structure on population clustering and connectivity in fragmented artesian spring snail populations

Many organisms occupy heterogeneous landscapes that contain both barriers to movement as well as corridors that facilitate dispersal. The extent to which such features determine population connectivity will depend on the mechanisms utilized by organisms to disperse. Here we examined the interaction between landscape structure and dispersal in the endemic aquatic snail, Fonscochlea accepta , in the fragmented artesian spring ecosystem of arid central Australia. We used frequentist and Bayesian analyses of microsatellite data to identify population structure and immigration for 1130 snails sampled from 50 springs across an entire spring complex. We introduce a modified isolation-by-distance analysis to test hypotheses about how populations are clustered and to distinguish the most likely dispersal pathways within and between those clusters. Highly significant differences in F _ST values and significant isolation-by-distance patterns were detected among springs across the entire complex, while Bayesian assignment tests revealed the presence of two hierarchical levels of spring clustering. Clusters were defined by the spatial aggregation of springs, dynamic aquatic habitat connections between springs and the ecology of the snails. Bayesian immigrant identification and our modified isolation-by-distance analysis revealed that dispersal occurs at two geographical scales via two very different mechanisms. Short range dispersal (usually ≤ 300 m) occurs via active movement facilitated by aquatic connections among springs while long-range dispersal (≥ 3 km) is likely facilitated by an animal vector (phoresy). These results underline the importance of both dispersal mode and landscape structure in influencing connectivity rates and patterns among populations.     

Strong spatial genetic structure in peripheral but not core populations of Sitka spruce [Picea sitchensis (Bong.) Carr.

We examined spatial genetic structure within eight populations of Sitka spruce classified as core or peripheral based on ecological niche, and continuous or disjunct based on species distribution. In each population, 200 trees were spatially mapped and genotyped for eight cDNA-based sequence tagged site (STS) codominant markers. Spatial autocorrelation was assessed by estimating p(ij), the average co-ancestry coefficient, between individuals within distance intervals. The distribution of alleles and genotypes within core populations was almost random, with nonsignificant co-ancestry values among trees as close as 50 m in core populations. In contrast, the distribution of alleles and genotypes within peripheral populations revealed an aggregation of similar multilocus genotypes, with co-ancestry values greater than 0.20 among trees up to 50 m apart and significant, positive values between trees up to 500 m. The relatively high density of reproductive adults in core populations may lead to highly overlapping seed shadows that limit development of spatial genetic structure. However, in peripheral populations with a lower density of adults, the distribution of alleles and genotypes was highly structured, likely due to offspring establishment near maternal trees and subsequent biparental inbreeding, as well as more recent population establishment at the leading edge of post-Pleistocene range expansion. Conserving genetic diversity in peripheral populations may require larger reserves for in situ conservation than required in core populations. These data on spatial genetic structure can be used to provide guidance for sampling strategies for both ex situ conservation and research collections.     

Spatially heterogeneous refugia and predation risk in intertidal salt marshes

The effect of habitat structure on interactions between predators and prey may vary spatially. In estuarine salt marshes, heterogeneity in refuge quality derives from spatial variation in vegetation structure and in tidal inundation. We investigated whether predation by blue crabs on periwinkle snails was influenced by distance from the seaward edge of the salt marsh and by characteristics of the primary habitat structure, smooth cordgrass ( Spartina alterniflora ). Spartina may provide refuge for snails and interfere with foraging by crabs. Furthermore, predation risk should decline with distance from the seaward edge because landward regions require more travel time for crabs during tidal inundation. We investigated these processes using a comparative survey of snails and habitat traits, an experiment that assessed the crab population and measured predation risk, and a size-structured model that estimated encounter rates. Taken together, these approaches indicated that predation risk for snails was lower where Spartina was present and was lower in a landward direction. Furthermore, Spartina architecture and distance from the seaward edge interacted. The strength of the predation gradient between seaward and landward regions of the marsh was greater where Spartina was tall or dense. These predation gradients emerge because vegetation and distance inland decrease encounter rates between crabs and snails. This study suggests that habitat modification, a process not uncommon in salt marshes, may have consequences for interactions among intertidal fauna.     

Factors determining the direction of ecological specialization in snail-feeding carabid beetles

A stout-slender dimorphism in body shape is observed among carabid beetles of the subtribe Carabina, which feed on land snails. We hypothesized that this dimorphism has resulted from divergent ecological specialization for feeding on different-sized land snails. Therefore, we examined whether the geographic variation in the body shape of Damaster blaptoides, a representative snail-feeding species in Japan, is correlated with the size of Euhadra, a genus of land snails frequently consumed by D. blaptoides. An analysis of beetle specimens from the whole distribution area of D. blaptoides determined that more slender beetle populations occurred in localities harboring larger snails, whereas more stout beetles inhabited localities harboring smaller snails. This pattern could be adaptive because slender beetles exhibit high feeding performance for large snails by inserting their heads into the shells, whereas stout beetles do so for small snails by crushing the shells. The D. blaptoides populations showed a clear genetic isolation-by-distance pattern, which could be effective in promoting such local adaptation. Thus, food resources as well as geographic isolation may have promoted adaptive divergence of external morphology in the snail-feeding carabid beetles.     

Modifications of Motor Asymmetry in Rats under the Influence of Low-Intensity Extra High-Frequency Electromagnetic Radiation in the Norm and under Stress Conditions

We studied modifications of motor asymmetry in rats with different motor lateralization (dextrals, sinistrals, and ambidextrals) induced by low-intensity extra high-frequency (EHF) electromagnetic radiation (EMR), hypokinetic stress, and their combination. It was found that the development of hypokinetic stress in rats induced by limitation of their mobility results in a considerable decrease of the coefficient of motor asymmetry (up to inversion of its sign); this can be related to a decrease in the resistivity to stressing and adaptability of the organism to the influence of external factors. The influence of EHF EMR on the animals under conditions of both normal and limited motor activity resulted in an increase in the index of motor lateralization in animals of all phenotypic groups under study; probably, this helped to increase the adaptive capabilities of the organism. Neirofiziologiya/Neurophysiology, Vol. 37, No. 2, pp. 164–168, March–April, 2005.     

Effect of immersion at low tide on distribution and movement of the mud snail, Ilyanassa obsoleta (Say), in the upper Bay of Fundy, eastern Canada

Habitat heterogeneity often affects movement behaviours of animals, and consequently their spatial distribution. We evaluated the effect of immersion at low tide on the distribution, fine-scale movement patterns and daily movement patterns of the mud snail Ilyanassa obsoleta on a mudflat in the upper Bay of Fundy, Canada. Mud snails migrate onto intertidal mudflats in the summer, and our field survey showed that their density was higher inside tide pools relative to adjacent areas that are exposed at low tide. Using time-lapse videography, we evaluated the effect of snail size, snail density, and immersion at low tide on fine-scale movement patterns of I. obsoleta. Time until snails stopped moving and burrowed was unaffected by snail size, but snails at low and high densities burrowed somewhat faster than those at intermediate densities. Snail size and snail density had no detectable effect on displacement speed or linearity of displacement. Immersion affected snail movement: snails within tide pools delayed burrowing and traveled in more convoluted paths compared to those on exposed mud. Snails increased their turning angles within tide pools, which is probably the mechanism by which aggregations are formed. We also performed a mark-recapture experiment to compare daily movement patterns of snails released inside and outside tide pools. Snails released in tide pools moved shorter distances, but did not orient themselves differently than snails released outside tide pools. Both groups exhibited significant directionality, moving against the mean water current direction over 24 h. In sum, immersion at low tide affected the behaviour and spatial distribution of snails, resulting in snail aggregations within tide pools. These snail aggregations, in turn, may be a major factor influencing spatial dynamics on mudflats, including causing changes in distribution patterns of the burrowing amphipod Corophium volutator, a dominant inhabitant and key species in the food web of mudflats.