Whole-Body Enantiomorphy and Maternal Inheritance of Chiral Reversal in the Pond Snail Lymnaea stagnalis

Abstract

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.

The development and evolution of left‐right asymmetry in invertebrates: Lessons from Drosophila and snails

“…Dextrality is genetically dominant in the mostly dextral families Lymnaeidae (Boycott et al, 1930;Asami et al, 2008) and Bradybaenidae (Ueshima and Asami, 2003). A dominance of sinistrality, however, has been confirmed in the Clausiliidae (Degner, 1952) and Partulidae (Murray and Clarke, 1976).…”

“…The direction of visceral asymmetry corresponds to the polarity of the primary asymmetry, which appears in early development (Levin, 2005;Sutcharit et al, 2007). A LR reversal of the primary asymmetry leads to polarity reversal throughout subsequent development, resulting in whole-body enantiomorphs, also referred to as situs inversus (Wood, 1991;Félix et al, 1996;Levin, 2005;Asami et al, 2008). Thus, although the details remain mostly unexplored, some cascade of polarity determinants must act between the advent of primary asymmetry and the final asymmetry of the body structure, including that of the visceral mass (whole-body asymmetry).…”

“…Efficient and comprehensive genetic studies on the mechanisms of asymmetry development can be performed using invertebrates, especially D. melanogaster (Hozumi et al, 2006;Spéder et al, 2006) and C. elegans (Bergmann et al, 2003;Poole and Hobert, 2006). In snails (Asami et al, 1998(Asami et al, , 2008Ueshima and Asami, 2003;Hierck et al, 2005) and nematodes (Félix et al, 1996), "mirror-image" enantiomorphs or species, which have evolved through LR reversal of the primary asymmetry in the wild, are available as laboratory lines. Such mirror-image specimens from the wild are not known among vertebrates.…”

The oldest evidence of non-coaxial shell heterostrophy in the Class Gastropoda

“…Additionally, many bilaterian groups, having an externally symmetrical body, exhibit bilateral asymmetry in shape and spatial arrangement of their internal organs. The origin and evolution of the asymmetry in the Bilateria is one of the frequently discussed topics of molecular and developmental biology (e.g., Asami et al 2008, Kuroda et al 2009, Hendricks 2009, Schilthuizen & Haase 2010. In the case of body asymmetry, two enantiomorphic body plans are possible, which are symmetrical with respect to the plane (e.g.…”

“…Ueshima & Asami (2003) showed that a single gene causes the mirror-image form of a gastropod body plan. Asami et al (2008) demonstrated, with crossing experiments, that the primary asymmetry of freshwater pulmonate Lymnaea stagnalis (Linnaeus, 1758) is determined by the maternal genotype at a single nuclear locus, where the dextral allele is dominant over the sinistral allele. Therefore, it is not the genotype of individual animals that determines the handedness of the shell; but rather, it is the genotype of the mother that determines the phenotype of her progeny.…”