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Am Nat. 1998 Aug;152(2):225-36. doi: 10.1086/286163.

Evolution of mirror images by sexually asymmetric mating behavior in hermaphroditic snails.

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  • 1Division of Biology, Tokyo Metropolitan College, Azuma-cho, Akishima-shi, Tokyo 196-8540, Japan.


Directionally asymmetric animals generally exhibit no variation in handedness of whole-body architecture. In contrast, reversed chirality in both coil and entire anatomy has frequently evolved in snails. We demonstrate a nonrandom pattern and deterministic process of chiral evolution, as predicted by the following hypothesis. Bimodal shell shapes are associated with discrete mating behaviors in hermaphroditic pulmonates. Flat-shelled species mate reciprocally, face-to-face. This sexual symmetry prevents interchiral mating because genitalia exposed by a sinistral on its left side cannot be joined with those exposed by a dextral on its right. Thus, selection against the chiral minority, resulting from mating disadvantage, stabilizes chiral monomorphism. Tall-shelled species mate nonreciprocally: the 'male' copulates by mounting the 'female's' shell, mutually aligned in the same direction. This sexual asymmetry permits interchiral copulation with small behavioral adjustments. Therefore, the positive frequency-dependent selection is relaxed, and reversal alleles persist longer in populations of tall-shelled species. We verified both the assumption and the prediction of this hypothesis: significantly lower interchiral mating success in a low-spired species and higher chiral evolution rate in high-spired taxa. Sexual asymmetry is the key to understanding the accelerated chiral evolution in high-spired pulmonates.

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