Abstract

Diverse animals exhibit left–right asymmetry in development. However, no example of dimorphism for the left–right polarity of development (whole-body enantiomorphy) is known to persist within natural populations. In snails, whole-body enantiomorphs have repeatedly evolved as separate species. Within populations, however, snails are not expected to exhibit enantiomorphy, because of selection against the less common morph resulting from mating disadvantage. Here we present a unique example of evolutionarily stable whole-body enantiomorphy in snails. Our molecular phylogeny of South-east Asian tree snails in the genus Amphidromus indicates that enantiomorphy has likely persisted as the ancestral state over a million generations. Enantiomorphs have continuously coexisted in every population surveyed spanning a period of 10 years. Our results indicate that whole-body enantiomorphy is maintained within populations opposing the rule of directional asymmetry in animals. This study implicates the need for explicit approaches to disclosure of a maintenance mechanism and conservation of the genus.

Highlights

  • Diverse groups of animals exhibit asymmetry in internal structure

  • Sequence divergence between the genus Amphidromus and each of the outgroups, Beddomea, Camaena and Chloritis ranged from 32.6% to 38.2%

  • Enantiomorphy is evolutionarily stable in Amphidromus, contrary to the prevailing view that chiral monomorphism for the primary asymmetry is the rule in snails as well as in other animals

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Summary

Introduction

Diverse groups of animals exhibit asymmetry in internal structure. Visceral asymmetry generally indicates the direction of primary asymmetry, which corresponds to the left–right polarity in early development (Crampton, 1894; Wood, 1997; Levin, 2005; Hozumi et al, 2006). In a variety of animals, mutation in molecular pathways controlling the direction of the primary asymmetry is known to produce whole-body enantiomorphs Possible reversal of the primary asymmetry would not be recognized unless developmental or visceral asymmetry is identified, even if external enantiomorphs are found such as in barnacles (Yusa et al, 2001). It is clear that the primary asymmetry does not generally exhibit chiral dimorphism (enantiomorphy), except for few groups (Felix et al, 1996; Asami et al, 1998)

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