Maternal Inheritance of Racemism in the Terrestrial Snail Bradybaena similaris

Abstract

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.

Shells and heart: Are human laterality and chirality of snails controlled by the same maternal genes?

“…Freeman and Lundelius [1982] showed, by cytoplasmic transplantation between eggs derived from pure dextral and sinistral strains in the normally dextral snail Lymnaea peregra, that cytoplasm of dextral eggs injected in sinistral eggs caused dextrality, but not vice versa. This demonstrated that in this right-handed species, the dextral allele is dominant to the sinistral allele, only the former producing a functioning dextral chiral determinant (although a rare ''racemic'' allele producing both enantiomorphs was found recently [Utsuno and Asami, 2010]). …”

Enantiomorphs differ in shape in opposite directions between populations

“…Accordingly, the present changes of polarity–shape relationship depending on population may reflect genetic differences in the epigenetic effect of early development on shape among populations. In support of this view, previous studies also suggested that the polarity of development affects embryonic viability in the land snails Bradybaena similaris (Rang) (Utsuno & Asami, 2010) and Hemizaptyx stimpsoni (Böttger) (Utsuno et al. , 2010).…”

“…This suggests that the polarity of development in this group is also determined by a maternal effect of the polarity gene as well as in four other superfamilies of pulmonates (Sturtevant, 1923; Degner, 1952; Murray & Clarke, 1976; Asami et al. , 2008; Utsuno & Asami, 2010).…”

Internal Selection Against the Evolution of Left-Right Reversal

“…Thus, there may be a substantial amount of genetic variation in the relative viability of sinistral embryos in the original wild population. Previous studies also suggested that polarity‐dependent differences in embryonic viability are genetically variable in two species of the different land‐snail families Bradybaenidae (Utsuno and Asami 2010) and Clausiliidae (Utsuno et al 2010). Similarly to the embryonic viability analysis, we found that the degree of interchiral difference in adult‐shell shape significantly depends on the parents, which suggest the presence of genetic variation in the degree of morphological differences between the morphs.…”

“…At least in pulmonate gastropods, spiral cleavage proceeds in opposite direction between dextral and sinistral species from the first cell cycle (Crampton 1894; Camey and Verdonk 1970; Meshcheryakov and Beloussov 1975). As shown in four phylogenetically independent families (Wade et al 2006; Okumura et al 2008; Utsuno and Asami 2010), the left–right polarity of development in pulmonates is determined by a maternal effect of a single nuclear gene (Fig. 1, Sturtevant 1923; Boycott et al 1930; Asami et al 2008) and thus exhibits maternal inheritance (Toyama 1913).…”