We found marked directional asymmetry in mandibular tooth number (left: 17.5±1.1, right: 24.9±1.1, n
) of a snail-eating specialist P. iwasakii
. This was established before hatching (left: 18, right: 26, n
=1) and showed no correlation with snout–vent length (Kendall's τ
=24). Thus, dentition asymmetry does not change through the ageing processes. The mandibles were clearly asymmetric in 12 out of 14 pareatine species examined (d
). However, the two species which are known to be non-snail-eating specialists (Stuebing & Inger 1999
) showed symmetry. Thus, the dentition asymmetry probably reflects dietary specialization on snails.
To determine whether the dentition asymmetry of P. iwasakii has been adapted specifically for the predation of dextral snails, we conducted feeding experiments using the dextral wild-type and sinistral variant of a land snail B. similaris. We found that the sinistral morph required significantly longer handling time than the dextral (four wild-captured snakes; REML GLMM, F1,84.4=41.3, p<0.0001; a) and more mandible retractions to complete soft-body extraction (F1,68.8=34.0, p<0.0001; b). The dentition asymmetry should, therefore, be an adaptation for improved performance in the extraction of the dextral soft body.
Figure 2 Feeding performance and success on dextral (filled circles) and sinistral (open circles) morphs of Bradybaena similaris by the four snakes of Pareas iwasakii. (a) Handling times, (b) the number of mandibular retractions for soft-body extraction (means±s.e.) (more ...)
Pareas iwasakii failed in the predation of sinistral snails more frequently than in the predation of dextrals (F=1, p=0.0006). The snakes showed obvious difficulties in holding sinistral prey because the upper jaws barely reached the outer shell surface on which the jaws need to anchor (video B of electronic supplementary material). This is the physically natural outcome of behavioural asymmetry when striking (a). They did not adjust striking behaviour for sinistral prey or recognize the direction of asymmetry of prey.
According to the phylogeny of the three pareatine genera (Rao & Yang 1992
), the dentition asymmetry is ancestral and the symmetry of slug eaters is secondarily derived. The symmetry break of snake dentition may have been a key innovation that initiated the adaptive radiation of pareatine snakes throughout Southeast Asia as dextral-snail eaters. Solid reconstruction of pareatine phylogeny is, however, necessary to validate this example against the general derivation of asymmetry from symmetry in animals (Palmer 1996
In addition, our experiments demonstrate a defensive function of sinistrality for snails against snake predators. Sinistral variants have been generally considered to suffer selective disadvantages on account of the overwhelming predominance of dextrals (Vermeij 1975
; Johnson 1982
; Gould et al. 1985
; Asami et al. 1998
; but see Dietl & Hendricks 2006
). However, sinistrals should enjoy a selective advantage over dextrals under chirally biased predation by snakes. The remarkable diversity of sinistral snails in Southeast Asia (Vermeij 1975
; Hoso et al
. 2006, unpublished data) may be attributable to ‘right-handed predation’ by the snakes.
Predation of land snails by soft-body extraction has been independently employed at least by three groups of colubrid snakes (Cundall & Greene 2000
). Among them, neotropical snail-eating snakes of the subtribe Dipsadini (genera Dipsas
) closely resemble pareatines in several character complexes including cranial morphology (Savitzky 1983
) and soft-body extracting behaviour by alternate mandible retraction (Sazima 1989
; Gotz 2002
). Their similarities may also suggest convergence of morphology and behaviour for the predation of dextral snails between tropic and neotropic snail-eating snakes.