Right-handed snakes: convergent evolution of asymmetry for functional specialization

External asymmetry found in diverse animals bears critical functions to fulfil ecological requirements. Some snail-eating arthropods exhibit directional asymmetry in their feeding apparatus for foraging efficiency because dextral (clockwise) species are overwhelmingly predominant in snails. Here, we show convergence of directional asymmetry in the dentition of snail-eating vertebrates. We found that snakes in the subfamily Pareatinae, except for non-snail-eating specialists, have more teeth on the right mandible than the left. In feeding experiments, a snail-eating specialist Pareas iwasakii completed extracting a dextral soft body faster with fewer mandible retractions than a sinistral body. The snakes failed in holding and dropped sinistral snails more often owing to behavioural asymmetry when striking. Our results demonstrate that symmetry break in dentition is a key innovation that has opened a unique ecological niche for snake predators.

[1]  Michael S. Johnson Polymorphism for direction of coil in Partula suturalis: Behavioural isolation and positive frequency dependent selection , 1982, Heredity.

[2]  C. Benkman Are the ratios of bill crossing morphs in crossbills the result of frequency-dependent selection? , 2005, Evolutionary Ecology.

[3]  A. R. Palmer,et al.  From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  G. Vermeij The Geography of Evolutionary Opportunity: Hypothesis and Two Cases in Gastropods1 , 2002, Integrative and comparative biology.

[5]  I. Sazima Feeding behavior of the snail-eating snake, Dipsas indica , 1989 .

[6]  R. Stuebing,et al.  A Field Guide to the Frogs of Borneo@@@The Natural History of Amphibians and Reptiles in Sabah , 1999 .

[7]  S. Gould,et al.  THE CONSEQUENCES OF BEING DIFFERENT: SINISTRAL COILING IN CERION , 1985, Evolution; international journal of organic evolution.

[8]  N. Snyder,et al.  A comparative study of mollusk predation by limpkins, Everglade kites, and boat-tailed grackles , 1969 .

[9]  D. Cundall CHAPTER 9 – Feeding in Snakes , 2000 .

[10]  Yusuke Shigemiya Does the handedness of the pebble crab Eriphia smithii influence its attack success on two dextral snail species , 2003 .

[11]  R. Stuebing,et al.  A field guide to the snakes of Borneo , 1999 .

[12]  M. Hori,et al.  Frequency-Dependent Natural Selection in the Handedness of Scale-Eating Cichlid Fish , 1993, Science.

[13]  Y. Hirata,et al.  Asymmetric Mandibles of Water‐Scavenger Larvae Improve Feeding Effectiveness on Right‐Handed Snails , 2003, The American Naturalist.

[14]  Kurt Schwenk,et al.  Feeding : form, function, and evolution in tetrapod vertebrates , 2000 .

[15]  G. Dietl,et al.  Crab scars reveal survival advantage of left-handed snails , 2006, Biology Letters.

[16]  G. Vermeij Evolution and distribution of left-handed and planispiral coiling in snails , 1975, Nature.

[17]  P. Ng,et al.  'Right Handedness' in Heterochelous Calappoid and Xanthoid Crabs - Suggestion for a Functional Advantage , 1985 .

[18]  A. Savitzky Coadapted Character Complexes Among Snakes: Fossoriality, Piscivory, and Durophagy , 1983 .

[19]  F. H. Pough,et al.  Specializations of the Body Form and Food Habits of Snakes , 1983 .

[20]  R. Cowie,et al.  Evolution of Mirror Images by Sexually Asymmetric Mating Behavior in Hermaphroditic Snails , 1998, The American Naturalist.

[21]  A. R. Palmer Symmetry Breaking and the Evolution of Development , 2004, Science.

[22]  J. B. Shoup,et al.  Shell Opening by Crabs of the Genus Calappa , 1968, Science.