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     

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.     

Sinistral snail shells in the sea: developmental causes and consequences

The paucity of sinistral (left-coiling) relative to dextral (right-coiling) species of gastropods in the marine realm is an enigma. In Conus , one of the most diverse marine animal genera, sinistral shell coiling has evolved as a species-wide character only once. Fossils of this species, Conus adversarius , are found in Upper Pliocene and lowermost Pleistocene deposits in the southeastern USA. Conus adversarius had nonplanktonic larval development; this may have been a critical factor for the early establishment of the species, as well as sinistral marine species in other clades. Notably, most specimens of aberrantly sinistral modern Conus are derived from typically dextral species that have nonplanktonic development. If C. adversarius was reproductively isolated from dextral conspecifics, then this species may provide an example of nearly instantaneous sympatric speciation in the fossil record. Furthermore, the common and widespread – while geologically short-lived – fossil shells of C. adversarius show large amounts of variability in form and this variation may be related, at least in part, to a pleiotropic effect associated with the reversed coiling direction of this species.     

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.     

Right-left symmetry preservation by flowers of malvaceae family

The flowers of malvaceae family preserves the symmetry between right and left in a peculiar manner. Plots belonging to this family bear two kinds of flowers, right-handed flowers with anticlockwise twisted petals and left-handed flowers with clockwise twisted petals. The branches of the plant prefers production of one type of flowers in excess of the other. There are two distinct types of branches, dextral branches and sinistral branches. Dextral (sinistral) branches produce more right-handed (left-handed) flowers than left-handed (right-handed) flowers. The average percentage of right-handed flowers in a dextral branch is same as that of left-handed flowers in a sinistral branch.     

Delayed prezygotic isolating mechanisms: evolution with a twist

Assortative mating characterizes the situation wherein reproducing individuals pair according to similarity. Usually, the impetus for this bias is attributed to some type of mate choice conferring benefits (e.g., increased fitness or genetic compatibility) and, thereby, promoting speciation and phenotypic evolution. We investigate, by computer simulation of an evolving deme-structured snail population, the ramifications ensuing from passive assortative mating wherein couples exhibiting opposite shell coil direction phenotypes experience a physical constraint on mating success: putative mating partners inhabiting stout dextral and sinistral shells are unable to exchange sperm. Because shell coil chirality genotype is encoded at a single locus by shell coil alleles that are inherited maternally, snails containing sinistral alleles can present the typical dextral phenotype. Consequently, the incidence of a sinistral allele in as few as one snail can be manifested as prezygotic reproductive isolation within a deme in a subsequent generation. However, because the efficacy of achieving this type of prezygotic reproductive isolation is affected by shell form, the likelihood and product of single-gene speciation should be determined by deme interaction (migration) and composition (morphological distribution). We test this hypothesis and show how stochastic migration interacts with passive assortative mating yielding morphologically induced prezygotic reproductive isolation to produce new species phenotypes. The results show that demes can achieve rapid macroscopic phenotypic transformation and indicate that sympatric speciation might be more plausible than naturalists recognize conventionally.     

Which way to turn? Effect of direction of body asymmetry on turning and prey strike orientation in starry flounder Platichthys stellatus (Pallas) (Pleuronectidae)

Starry flounder Platichthys stellatus , a rare polymorphic flatfish exhibiting a large-scale geographic cline in the frequency of right-eyed (dextral) and left-eyed (sinistral) morphs, was studied to investigate whether foraging behaviour (turning angle and prey strike orientation) differed between dextral and sinistral laboratory-raised juveniles. Platichthys stellatus foraging on brine shrimp Artemia sp. nauplii tended to strike dorsally at prey ('left' to an observer for dextral flounder and 'right' to an observer for sinistral flounder), although this effect was stronger for sinistral fish. This dorsal tendency also increased with body size. Non-strike behaviours (movements between strikes) were ventrally biased for both morphs. Maximum turn angles were larger for both morphs towards the dorsal side than the ventral side during prey strikes but were the same during non-strike behaviours. The positioning of the eyes of the juvenile starry flounder was skewed towards the dorsal midline rather than being symmetrically placed between dorsal and ventral margins on the eyed side of each fish. The migrating eyes of dextral fish, however, were significantly closer to the dorsal midline than in sinistral fish. This, in addition to the more dorsally oriented prey strikes in sinistral fish, suggests that the morphs are not simple behavioural mirror images of one another and therefore may differ ecologically.     

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.     

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).     

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.     

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.     

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.     

Spirorbinae (Polychaeta: Serpulidae) of the Galapagos Islands*

Twelve species, six of which are new, are recorded from shores andshallow water. The most generally abundant are Spirorbis tricornigerus Rioja, S. bushi Rioja (both dextral with tube incubation), S. regalis sp. n., S. tuberculatus sp. n. (both sinistral with opercular incubation) and S. placophora sp. n. (sinistral, with tube incubation). Other sinistral species include S. claparedei Caullery & Mesnil, S. berkeleyana Rioja, S. bidentatus sp. n., and S. translucens sp. n. Dextral species include S. marioni Caullery & Mesnil, S. pagenstecheri Quatrefages and S. unicornis sp. n. The new species mentioned above have been described by the author named first.
The Spirorbis fauna seems to be quite like that of Mexico and S. America, from which repeated introductions have probably occurred, perhaps on stones buoyed by seaweeds and drifting on the Peruvian and El Nino currents. Its considerable diversity is not attributed to speciation within the archipelago.     

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.     

Phylogeography of the land snail Albinaria hippolyti (Pulmonata: Clausiliidae) from Crete, inferred from ITS-1 sequences

The polytypic Cretan land snail Albinaria hippolyti has a range that is partly fragmented and partly subdivided by hybrid zones. For this reason, it has served as a model species for investigating speciation and radiation in Mediterranean Clausiliidae. The first internal transcribed spacer ( ITS-1 ) of the nuclear ribosomal DNA was sequenced in 20 populations of A. hippolyti and phylogenetically analysed using maximum parsimony. We employed a novel method involving logarithmic weighting of gaps and topological constraints based on bootstrap values. The resulting phylogeography suggests that the species has undergone a recent cycle of range expansion and range reduction. Speciation cannot be linked to major geological vicariance events in the Miocene and Pliocene, as has been suggested previously. The subspecies A. h. arthuriana appears unrelated to other A. hippolyti subspecies, which supports recent suggestions, based on morphology, to regard it as a separate species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 317–326.     

Chirally dimorphic male genitalia in praying mantids (Ciulfina: Liturgusidae)

Although male polymorphisms occur widely in nature and have received considerable recent attention from studies of alternative mating strategies, male genital polymorphisms are less well known. Here, we describe a dimorphism in the orientation of the male genitalic complex of the praying mantid genus Ciulfina. Populations of Ciulfina species vary in the proportion of males with dextral (right‐oriented) and sinistral (left‐oriented) genitalia, ranging from directional asymmetry (single orientation only) to apparent antisymmetry (equal proportions of both orientations). The proportion of dextral males varied between species (C. baldersoni: 46%; C. rentzi: 24%; C. klassi: 100%; C. biseriata: 83%) and between populations. We used elliptic Fourier analysis to quantify shape and size variation between the genitalia of dextral and sinistral males and determined that the two forms were mirror images of one another in two species. We found that the level of mechanical reproductive isolation between heterospecific populations of opposite genital orientation was no greater than that between heterospecific populations with the same orientation or of mixed orientation. Genital orientation therefore did not influence premating isolation between these species, despite complete postmating isolation. The geographic proximity of populations to heterospecifics also showed no particular pattern with respect to genital orientation. These results suggest that reversible trait asymmetry in Ciulfina is not driven by reproductive isolation, and add to the growing evidence against the species isolation hypothesis for rapid genital evolution. J. Morphol. 271:1176–1184, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

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.     

Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo

Although substantial progress has been made recently in understanding the establishment of left-right asymmetry in several organisms, little is known about the initial step for any embryo. In gastropods, left-right body handedness is determined by an unknown maternally inherited single gene or genes at closely linked loci and is associated with the sense of spiral cleavage in early embryos. Contrary to what has been believed, we show that temporal and spatial cytoskeletal dynamics for the left- and right-handed snails within a species are not mirror images of each other. Thus, during the third cleavage of Lymnaea stagnalis, helical spindle inclination (SI) and spiral blastomere deformation (SD) are observed only in the dominant dextral embryos at metaphase-anaphase, whereas in the recessive sinistral embryos, helicity emerges during the furrow ingression. Actin depolymerization agents altered both cleavages to neutral. Further, we found a strong genetic linkage between the handedness-specific cytoskeletal organization and the organismal handedness, using backcrossed F4 congenic animals that inherit only 1/16 of dextral strain-derived genome either with or without the dextrality-determining gene(s). Physa acuta, a sinistral-only gastropod, exhibits substantial SD and SI levotropically. Thus, cytoskeletal dynamics have a crucial role in determination of body handedness with further molecular, cellular, and evolutionary implications.     

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.