The unique nature of body handedness, which is distinct from the anteroposterior and dorsoventral polarities, has been attracting growing interest in diverse biological disciplines. Recent research progress on the left-right asymmetry of animal development has focused new attention on the mechanisms underlying the development and evolution of invertebrate handedness. This exploratory review of currently available information illuminates the prospective value of Drosophila and pulmonate snails for innovative new research aimed at elucidating these mechanisms. For example, findings in Drosophila and snails suggest that an actin filament-dependent mechanism may be evolutionarily conserved in protostomes. The polarity conservation of primary asymmetry across most metazoan phyla, which visceral handedness represents, indicates developmental constraint and purifying selection as possible but unexplored mechanisms. Comparative studies using Drosophila and snails, which have the great advantages of using genetic and evolutionary approaches, will accelerate our understanding of the mechanisms governing the conservation and diversity of animal handedness. Developmental Dynamics 237: 3497-3515, 2008.

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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.K E Y W O R D S : Chirality, homochirality, maternal epistasis, maternal inheritance, maternal pleiotropy, situs inversus.

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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.

In metazoan animals, almost every known mutation of visceral asymmetry, which presents the polarity of primary asymmetry established in early development, reverses development in only about half or fewer of homozygotes. However, in pulmonate snails, the dextral and sinistral alleles are traditionally known to determine the polarity of offspring with complete dominance, and thus, each parent should produce either dextral or sinistral progeny. Contrary to this expectation, we found a mutant that produces both chiral morphs (enantiomorphs) within the same clutches in Bradybaena similaris. This study demonstrates that the consistent production of both enantiomorphs is determined by a maternal effect of a recessive allele, which probably randomizes the polarity. In snails that copulate simultaneously and reciprocally, a left-right reversed strain cannot usually be established or rescued from inbreeding depression by ad hoc outbreeding because a rarely found single mutant cannot reproduce due to great difficulties of mating with the wild type and selfing. Moreover, the rare recessive homozygote cannot easily be detected because it often exhibits the wild-type phenotype in maternal inheritance and breeding difficulty hampers genotyping it by phenotyping its progeny. The present strain established by virtue of rare advantages will, therefore, provide unique opportunities to investigate whole-body enantiomorphs.

Depending on fitness consequences, hybridization may rescue inbred populations; generate premating barriers, reproductive interference, or hybrid species; or extinguish a species. However, the fitness of hybrids is unpredictable without direct quantification of their performance in fitness components across multiple generations. The land snails Bradybaena pellucida and B. similaris, which are indigenous and non-indigenous in Japan, respectively, copulate with each other simultaneously and reciprocally. However, only B. pellucida produces hybrids, because it ends mating by removing the penis before transferring a spermatophore, while B. similaris inseminates B. pellucida. To evaluate the strength of an intrinsic postzygotic barrier against the hybrids produced by B. pellucida, we conducted breeding experiments in the laboratory and measured six life-history traits: (1) growth rate, (2) body weight at maturity, (3) number of days to first oviposition after being permitted to mate, (4) clutch size, (5) fecundity, and (6) hatchability. We also calculated the relative intrinsic fitness based on five of these trait values (excluding clutch size). F1 hybrids exhibited heterosis in growth rate, body weight at maturity and relative intrinsic fitness. F2 hybrids also showed heterosis in body weight at maturity. Nevertheless, the F2 hybrids produced significantly fewer progeny than the mid-point value of the parental species. Thus, the F2 hybrids exhibited weak outbreeding depression in reproduction, offsetting their vigor in body size. These results indicate that only a weak postzygotic barrier, contrasting with strong F1 heterosis, has evolved during genetic divergence of the two sibling species in allopatry.

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