Reproductive character displacement by inversion of coiling in clausiliid snails (Gastropoda, Pulmonata)

In land snails, a change in the direction of coiling, being associated with a shift in the position of the genital apparatus, may act as a barrier against hybridization between sympatric species. Putative reproductive character displacement by an inversion in chirality has been reported in only a few land snails, based on observations in the field and interbreeding experiments. In this study, we present a new case of possible reproductive character displacement in the direction of coiling, in the clausiliid snail Isabellaria dextrorsa . This species is dextral, in contrast with its nearest relatives, including I. torifera and I. lophauchena , which share plesiomorphic sinistral coiling. Whereas I. dextrorsa occurs in sympatry and even syntopically with I. lophauchena throughout most of its range, the sinistral species have a mosaic distribution. Phylogenetic analyses of mitochondrial cytochrome c oxidase subunit I (COI) sequences demonstrated that I. dextrorsa constitutes a clade with I. torifera . In this clade, a shift in coiling direction occurred at least twice, maybe triggered by the presence of a sympatric congeneric sinistral species. The analyses separated the sequences of all I. dextrorsa samples from those of sympatric and syntopic I. lophauchena samples. The failure to demonstrate gene flow between these species is consistent with the hypothesis of genetic isolation by reproductive character displacement.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 155–164.     

Chiral speciation in terrestrial pulmonate snails

On the basis of data in the literature, the percentages of dextral versus sinistral species of snails have been calculated for western Europe, Turkey, North America (north of Mexico), and Japan. When the family of Clausiliidae is represented, about a quarter of all snail species may be sinistral, whereas less than one per cent of the species may be sinistral where that family does not occur. The number of single-gene speciation events on the basis of chirality, resulting in the origin of mirror image species, is not closely linked to the percentage of sinistral versus dextral species in a particular region. Turkey is nevertheless exceptional by both a high percentage of sinistral species and a high number of speciation events resulting in mirror image species. Shell morphology and genetic background may influence the ease of chirality-linked speciation, whereas sinistrality may additionally be selected against by internal selection. For the Clausiliidae, the fossil record and the recent fauna suggest that successful reversals in coiling direction occurred with a frequency of once every three to four million years.     

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.     

Patterns of cladogenesis in the venomous marine gastropod genus Conus from the Cape Verde islands

Isolated oceanic archipelagos are excellent model systems to study speciation, biogeography, and evolutionary factors underlying the generation of biological diversity. Despite the wealth of studies documenting insular speciation, few of them focused on marine organisms. Here, we reconstruct phylogenetic relationships among species of the marine venomous gastropod genus Conus from the Cape Verde archipelago. This small island chain located in the Central Atlantic hosts 10% of the worldwide species diversity of Conus. Analyses were based on mtDNA sequences, and a novel nuclear marker, a megalin-like protein, member of the low-density lipoprotein receptor gene family. The inferred phylogeny recovered two well-defined clades within Conus. One includes Cape Verde endemic species with larger shells, known as the "venulatus" complex together with C. pulcher from the Canary Islands. The other is composed of Cape Verde endemic and West Africa and Canary Island "small" shelled species. In both clades, nonendemic Conus were resolved as sister groups of the Cape Verde endemics, respectively. Our results indicate that the ancestors of "small" and "large" shelled lineages independently colonized Cape Verde. The resulting biogeographical pattern shows the grouping of most Cape Verde endemics in monophyletic island assemblages. Statistical tests supported a recent radiation event within the "small shell" clade. Using a molecular clock, we estimated that the colonization of the islands by the "small" shelled species occurred relatively close to the origin of the islands whereas the arrival of "large" shelled Conus is more recent. Our results suggest that the main factor responsible for species diversity in the archipelago may be allopatric speciation promoted by the reduced dispersal capacity of nonplanktonic lecithotrophic larvae.     

Curious chiral cases of caddisfly larvae: handed behavior, asymmetric forms, evolutionary history

Studies of right-left asymmetries have yielded valuable insights into the mechanisms of both development and evolution. Larvae from several groups of caddisflies (Trichoptera) build portable asymmetrical cases within which they live. In nearly all species that build spiral-walled tubular cases, the direction of wall coiling is random (equal numbers of dextral and sinistral cases within species) whereas in all species that build helicospiral, snail-like cases the direction of coiling is exclusively dextral. Asymmetrical tubes result from handed behavior, and ～20% of larvae removed from a spiral-walled, tubular case build a replacement case of opposite chirality. So handed behavior (and hence direction of tube-wall spiraling) is likely learned rather than determined genetically. Asymmetrical larval cases appear to have evolved at least seven times in the Trichoptera, five times as spiral-walled tubes and twice as snail-like helicospiral cases. Helicospiral cases may reduce vulnerability to predation by mimicking snail shells, whereas spiral arrangements of vegetation fragments in tube walls may be more robust mechanically than other arrangements, but experimental evidence is lacking. Within one family (Phryganeidae), one or perhaps two species exhibit an excess of sinistral-walled cases, suggesting that genes that bias handed behavior in a particular direction evolved after handed behaviors already existed (genetic assimilation).     

Whole-body enantiomorphy and maternal inheritance of chiral reversal in the pond snail Lymnaea stagnalis

Sinistral and dextral snails have repeatedly evolved by left-right reversal of bilateral asymmetry as well as coiling direction. However, in most snail species, populations are fixed for either enantiomorph and laboratory breeding is difficult even if chiral variants are found. Thus, only few experimental models of chiral variation within species have been available to study the evolution of the primary asymmetry. We have established laboratory lines of enantiomorphs of the pond snail Lymnaea stagnalis starting from a wild population. Crossing experiments demonstrated that the primary asymmetry of L. stagnalis is determined by the maternal genotype at a single nuclear locus where the dextral allele is dominant to the sinistral allele. Field surveys revealed that the sinistral allele has persisted for at least 10 years, that is, about 10 generations. The frequency of the sinistral allele showed large fluctuations, reaching as frequent as 0.156 in estimate under the assumption of Hardy-Weinberg equilibrium. The frequency shifts suggest that selection against chiral reversal was not strong enough to counterbalance genetic drift in an ephemeral small pond. Because of the advantages as a model animal, enantiomorphs of L. stagnalis can be a unique system to study aspects of chirality in diverse biological disciplines.     

Evolution of a dextral lineage by left–right reversal in Cristataria (Gastropoda,Pulmonata, Clausiliidae)

It has long been debated whether mirror image‐like similarity in shell morphology between enantiomorphic pairs of dextral and sinistral taxa represents their sister relationship, or each of them is closer related to other congeners with the same coiling direction. The obligate rock‐dwelling genus Cristataria Vest, 1867 of the eastern Mediterranean region belongs to the Alopiinae subfamily of door snails (Clausiliidae). Cristataria and a few other genera of this subfamily include enantiomorphic pairs that are conchologically very similar to each other. Dextral C. colbeauiana (Pfeiffer, 1861) and its sinistral counterpart of such an enantiomorphic pair occur nearby one another in southern Turkey. However, the latter has been classified either as the sinistral subspecies C. colbeauiana inversa Szekeres, 1998 or as a form of sinistral C. leprevieri (Pallary, 1922). To examine the phylogenetic relationship of this enantiomorphic pair, we carried out molecular phylogenetic analysis of all the Turkish and two other Cristataria taxa based on both mitochondrial and nuclear DNA markers. Our results show that dextral C. colbeauiana and its sinistral counterpart are closest related to one another. This supports the classification of this enantiomorphic pair as dextral C. colbeauiana colbeauiana and sinistral C. colbeauiana inversa. Our results also reveal that these taxa and C. intersita Németh & Szekeres, 1995, sharing a characteristic collar behind the aperture of the shell, represent a monophyletic lineage. By contrast, the Cristataria species of non‐collared shells belong to another clade.     

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.     

The developmental genetics of dextrality and sinistrality in the gastropodLymnaea peregra

Summary The genetics of body asymmetry inLymnaea peregra follows a maternal mode of inheritance involving a single locus with dextrality being dominant to sinistrality. Maternal inheritance implies that all members of a brood have the same phenotype, however, some broods contain a few individuals of opposite coil. One purpose of this paper is to explain the origin of these anomalous individuals. Genetic analyses of sinistral broods with a few dextral individuals have led to the development of a cross-over model, with the anomalous dextrals originating as a consequence of crossing over either during meiosis or mitosis in the female germ line. The crossover either reconstitutes the dextral gene from previously dissociated parts, or creates a dextral gene by means of a position effect. The probability of a crossover event depends upon the appropriate combination of complementary sinistral chromosomes. Each crossover event has the potential of creating a unique dextral gene. Genetic analyses of dextral broods containing a few sinistral individuals have demonstrated that different dextral genes vary in penetrance.The dextral gene produces a product during oogenesis which influences the pattern of cleavage in the embryo; this cleavage pattern is translated into the appropriate body asymmetry. The other purpose of this paper is to provide an assay for this gene product. Cytoplasm from dextral eggs injected into uncleaved sinistral eggs causes these eggs to cleave in a dextral pattern. Cytoplasm from sinistral eggs has no effect on the cleavage pattern of dextral eggs. While the dextral gene product is made during oogenesis, it does not function in controlling cleavage until just before this process begins.     

New insights in late Miocene lower Chelif basin biostratigraphy based on planktonic foraminifera (Algeria)

Quantitative and qualitative analyses based on planktonic foraminifera of two sections (Oued Derdoussa and Djebel Meni) from lower Chelif basin (northern Algeria) enable us to identify for the first time a sequence of bioevents calibrated with the geomagnetic polarity time scale. The identified bioevents of late Miocene formations are useful for a high-resolution correlation in the whole western Mediterranean at local and regional scales. In particular, this work reveals that the sequence covers an interval of time that extends from the upper Tortonian up to the pre-evaporite Messinian period. Indeed, the base of the succession starts with a change in the coiling direction (from dextral to sinistral) of Neogloboquadrina acostaensis as the first bioevent. This later corresponds to the bioevent (1–8) assigned to the Tortonian sediments. This period is marked by the presence of Globorotalia menardii in sinistral coiled form that was substituted gradually with dextral coiled. The Tortonian/Messinian (T/M) boundary coincides to some extent with a sharp replacement of G. menardii group (I and II) with the first common occurrence (FCO) of Globorotalia miotumida plexus few meters below the development of the Tripoli diatomite formation (bioevent 9). This later is dominated mainly by highly convex species (G. miotumida plexus) marked by the presence of Globorotalia mediterranea in contrast with the marly formation at the base of the section. In this part, the recorded bioevents (10 to 17) are assigned to the Messinian sediments. Thus, the Tripoli formation shows the influx of Globorotalia nicolae and a small incursion of the dextrally coiled of Globorotalia scitula at the top of Oued Derdoussa section as a local bioevent that may be related to the local palaeoenvironment. We notice the absence of the change in the coiling from sinistral to dextral of N. acostaensis during the upper Messinian, this may be due to the coincidence of this bioevent with the barren levels.     

Phylogenetic reconstruction and shell evolution of the Diplommatinidae (Gastropoda: Caenogastropoda)

The fascinating and often unlikely shell shapes in the terrestrial micromollusc family Diplommatinidae (Gastropoda: Caenogastropoda) provide a particularly attractive set of multiple morphological traits to investigate evolutionary patterns of shape variation. Here, a molecular phylogenetic reconstruction, based on five genes and 2700 bp, was undertaken for this family, integrated with ancestral state reconstruction and phylogenetic PCA of discrete and quantitative traits, respectively. We found strong support for the Diplommatininae as a monophyletic group, separating the Cochlostomatidae into a separate family. Five main clades appear within the Diplommatininae, corresponding with both coiling direction and biogeographic patterns. A Belau clade (A) with highly diverse (but always sinistral) morphology comprised Hungerfordia, Palaina, and some Diplommatina. Arinia (dextral) and Opisthostoma (sinistroid) are sister groups in clade B. Clade C and D solely contain sinistral Diplommatina that are robust and little ornamented (clade C) or slender and sculptured (clade D). Clade E is dextral but biogeographically diverse with species from all sampled regions save the Caroline Islands. Adelopoma, Diplommatina, Palaina, and Hungerfordia require revision to allow taxonomy to reflect phylogeny, whereas Opisthostoma is clearly monophyletic. Ancestral state reconstruction suggests a sinistral origin for the Diplommatinidae, with three reversals to dextrality.     

Molecular phylogeny of the land snail genus Alopia (Gastropoda: Clausiliidae) reveals multiple inversions of chirality

Whereas the vast majority of gastropods possess dextral shell and body organization, members of the Clausiliidae family are almost exclusively sinistral. Within this group a unique feature of the alpine genus Alopia is the comparable representation of sinistral and dextral taxa, and the existence of enantiomorph taxon pairs that appear to differ only in their chirality. We carried out a molecular phylogenetic study, using mitochondrial cytochrome c oxidase subunit I (COI) gene sequences, in order to find out whether chiral inversions are more frequent in this genus than in other genera of land snails. Our results revealed multiple independent inversions in the evolutionary history of Alopia and a close genetic relationship between members of the enantiomorph pairs. The inferred COI phylogeny also provided valuable clues for the taxonomic division and zoogeographical evaluation of Alopia species. The high number of inverse forms indicates unstable fixation of the coiling direction. This deficiency and the availability of enantiomorph pairs may make Alopia species attractive experimental models for genetic studies aimed at elucidating the molecular basis of chiral stability. © 2013 The Linnean Society of London     

Shell chirality in Cambrian gastropods and sinistral members of the genus <Emphasis Type="Italic">Aldanella</Emphasis> Vostokova, 1962

Shell chirality among Cambrian gastropods is discussed. It is demonstrated that the earliest members of the class include chiral aberrations with abnormal opposite coiling of the shell. It is assumed that, in Cambrian gastropods, speciation could have occurred by mutation in the locus determining the chirality, as is proposed for extant gastropods. In contrast to modern gastropods, the existence of chiral morphs within single species has not been recorded in Cambrian mollusks, whereas the presence of chiral twin species is possible. The systematic position of sinistral representatives of the genus Aldanella Vostokova, 1962 is considered. Aldanella golubevi sp. nov. with sinistral shell is described from the base of the Tommotian Stage of the Anabar Region. Aberrant sinistral specimens of the normally dextral species Aldanella utchurica Missarzhevsky in Rozanov et al., 1969 and Pelagiella adunca Missarzhevsky in Rozanov et al., 1969 are figured.     

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.     

Morphological evidence of correlational selection and ecological segregation between dextral and sinistral forms in a polymorphic flatfish, Platichthys stellatus

Phenotypic polymorphisms in natural systems are often maintained by ecological selection, but only if niche segregation between morphs exists. Polymorphism for eyed-side direction is rare among the approximately 700 species of flatfish (Pleuronectiformes), and the evolutionary mechanisms that maintain it are unknown. Platichthys stellatus (starry flounder) is a polymorphic pleuronectid flatfish exhibiting large, clinal variation in proportion of left-eyed (sinistral) morphs, from 50% in California to 100% in Japan. Here I examined multiple traits related to swimming and foraging performance between sinistral and dextral morphs of P. stellatus from 12 sites to investigate if the two morphs differ in ways that may affect function and ecology. Direction of body asymmetry was correlated with several other characters: on an average, dextral morphs had longer, wider caudal peduncles, shorter snouts and fewer gill rakers than sinistral morphs. Although the differences were small in magnitude, they were consistent in direction across samples, implying that dextral and sinistral starry flounder may be targeting different prey types. Morphological differences between morphs were greatest in samples where the chances of competitive interactions between them were the greatest. These results suggest that the two morphs are not ecologically identical, may represent a rare example of divergent selection maintaining polymorphism of asymmetric forms, and that correlational selection between body asymmetry and other characters may be driven by competitive interactions between sinistral and dextral flatfish. This study is one of very few that demonstrates the ecological significance of direction in a species with polymorphic asymmetric forms.     

Dextral and sinistral <Emphasis Type="Italic">Amphidromus inversus</Emphasis> (Gastropoda: Pulmonata: Camaenidae) produce dextral sperm

Coiling direction in pulmonate gastropods is determined by a single gene via a maternal effect, which causes cytoskeletal dynamics in the early embryo of dextral gastropods to be the mirror image of the same in sinistral ones. We note that pulmonate gastropod spermatids also go through a helical twisting during their maturation. Moreover, we suspect that the coiling direction of the helical elements of the spermatozoa may affect their behaviour in the female reproductive tract, giving rise to the possibility that sperm chirality plays a role in the maintenance of whole-body chiral dimorphism in the tropical arboreal gastropod Amphidromus inversus (Müller, 1774). For these reasons, we investigated whether there is a relationship between a gastropod’s body chirality and the chirality of the spermatozoa it produces. We found that spermatozoa in A. inversus are always dextrally coiled, regardless of the coiling direction of the animal itself. However, a partial review of the literature on sperm morphology in the Pulmonata revealed that chiral dimorphism does exist in certain species, apparently without any relationship with the coiling direction of the body. Though our study shows that body and sperm chirality follows independent developmental pathways, it gives rise to several questions that may be relevant to the understanding of the chirality of spermatid ultrastructure and spermatozoan motility and sexual selection.     

Disassociation between weak sexual isolation and genetic divergence in a hermaphroditic land snail and implications about chirality

Examination of the association between reproductive isolation and genetic divergence in a variety of organisms is essential for elucidating the mechanisms causing speciation. However, such studies are lacking for hermaphrodites. We measured premating (sexual) isolation in species pairs of the hermaphroditic land snail Albinaria and we compared it with their genetic divergence. We did not find substantial sexual isolation barriers between the species studied. The absence of strong sexual isolation between species implies its minor effect in the evolution of this genus, because distributional, population and life-history characteristics of Albinaria make mate-choice possibly redundant. Furthermore, we found disassociation between genetic divergence and sexual isolation, suggesting that they do not form necessarily a cause-effect duet. However, Albinaria voithii, the only dextral Albinaria species, shows strong sexual isolation against the other sinistral species. We discuss whether change in coiling either has triggered instantaneous speciation, or is an example of character displacement.     

High gene flow despite opposite chirality in hybrid zones between enantiomorphic door snails

We studied differentiation and geneflow patterns between enantiomorphic door‐snail species in two hybrid zones in the Bucegi Mountains (Romania) to investigate the effects of intrinsic barriers (complications in copulation) and extrinsic selection by environmental factors. A mitochondrial gene tree confirmed the historical separation of the examined populations into the dextral Alopia livida and the sinistral Alopia straminicollis in accordance with the morphological classification, but also indicated gene flow between the species. By contrast, a network based on amplified fragment length polymorphisms (AFLP) markers revealed local groups of populations as units independent of their species affiliation. Admixture analyses based on AFLP data showed that the genomes of most individuals in the hybrid zones are composed of parts of the genomes of both parental taxa. The introgression patterns of a notable fraction of the examined markers deviated from neutral introgression. However, the patterns of most non‐neutral markers were not concordant between the two hybrid zones. There was also no concordance between non‐neutral markers in the two genomic clines and markers that were correlated with environmental variables or markers that were correlated with the proportion of dextral individuals in the populations. Neither extrinsic selection by environmental factors nor intrinsic barriers resulting from positive frequency‐dependent selection of the prevailing coiling direction were sufficient to maintain the distinctness of A. straminicollis and A. livida. Despite being historically separated units, we conclude that these taxa now merge where they come into contact.     

Asymmetrical rotations of blastomeres in early cleavage of gastropoda

Summary The movements of blastomere surfaces marked with carbon particles during cytokinesis of the Ist–IVth cleavage divisions in the eggs of the gastropodsLymnaea stagnalis, L. palustris, Physa acuta and Ph. fontinalis have been studied by time-lapse cinematographic methods. The vitelline membrane was removed with trypsin. At 2- and 4-cell stages shifts of nuclei have also been studied.Symmetrical as well as asymmetrical surface movements (in respect to the furrow plane) have been revealed. Symmetrical surface movements at the beginning of cytokinesis consist mainly in contraction of the furrow zone and in expansion of the more peripheral regions; between these there is a stationary zone. After the end of cytokinesis the furrow region expands.Considerableasymmetrical surface movements have also been observed in all four divisions. From anaphase until the end of cytokinesis each of the two sister blastomeres rotates with respect to the other in such a way, that if viewed along the spindle axis, the blastomere nearest to the observer rotates dexiotropically in a dextral species and laeotropically in a sinistral species (primary rotations). After the completion of cytokinesis the blastomeres may rotate in a reverse direction. The latter rotations are less pronounced in the IInd and IIIrd divisions and most pronounced in the IVth division. Blastomeres with the vitelline membrane intact retain a slight capacity for primary rotations. In normal conditions nuclei of the first two blastomeres shift mainly laeotropically in dextral species, but dexiotropically in sinistral species, being carried along by the reverse surface rotations.The invariable primary asymmetrical rotations of blastomeres seem to be the basis of enantiomorphism in molluscan cleavage. They are assumed to be determined by an asymmetrical structure of the contractile ring carrying out the cytokinesis.