Evolution of whole‐body enantiomorphy in the tree snail genus Amphidromus

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.

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

“…The Clausiliidae is one of the unusual families that are almost entirely sinistral. Sinistral, dextral, and enantiomorphic species have evolved in the Partulidae (Crampton, 1916(Crampton, , 1932, Achatinellidae (Welch, 1938(Welch, , 1942(Welch, , 1954 and Camaenidae (Sutcharit and Panha, 2006;Sutcharit et al, 2007). In the genus Partula, however, dextrality is dominant in F 2 and F 3 hybrids of the dextral P. mirabilis and the sinistral P. tohiveana olympia (Murray and Clarke, 1980).…”

“…The polarity of the secondary asymmetry develops independently of the polarity of the primary asymmetry (Sutcharit et al, 2007). For example, the polarity of the visceral asymmetry is not reversed between individuals showing specific enantiomorphic phenotypes in diverse species, including lobsters with reversed claws (Govind, 1989), flounders with reversed eyes (Policansky, 1982), and nematodes with a reversed cuticle (Bergmann et al, 1998).…”

“…For example, the polarity of the visceral asymmetry is not reversed between individuals showing specific enantiomorphic phenotypes in diverse species, including lobsters with reversed claws (Govind, 1989), flounders with reversed eyes (Policansky, 1982), and nematodes with a reversed cuticle (Bergmann et al, 1998). The most critical and obvious difference between primary and secondary asymmetry is in the level of evolutionary conservation against polarity reversal (Sutcharit et al, 2007). Secondary asymmetry has evolved within and between species far more frequently through symmetry breakdown or through polarity reversal than has primary asymmetry (Palmer, 2004;Levin and Palmer, 2007;Huber et al, 2007).…”

“…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).…”

“…Fluctuating asymmetry (van Valen, 1962;Polak, 2003) refers to random individual variation in the amount of difference between the right and left sides of a trait that is symmetric in the population mean. Enantiomorphy (Palmer, 2005;Sutcharit et al, 2007;Schilthuizen et al, 2007;Schilthuizen, 2007) is chiral dimorphism in which the dextral and sinistral morphs coexist in a population. Directional asymmetry is chiral monomorphism in which a population is fixed for either enantiomorph.…”