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A snail-eating snake recognizes prey handedness.

ABSTRACT: Specialized predator-prey interactions can be a driving force for their coevolution. Southeast Asian snail-eating snakes (Pareas) have more teeth on the right mandible and specialize in predation on the clockwise-coiled (dextral) majority in shelled snails by soft-body extraction. Snails have countered the snakes' dextral-predation by recurrent coil reversal, which generates diverse counterclockwise-coiled (sinistral) prey where Pareas snakes live. However, whether the snake predator in turn evolves any response to prey reversal is unknown. We show that Pareas carinatus living with abundant sinistrals avoids approaching or striking at a sinistral that is more difficult and costly to handle than a dextral. Whenever it strikes, however, the snake succeeds in predation by handling dextral and sinistral prey in reverse. In contrast, P. iwasakii with little access to sinistrals on small peripheral islands attempts and frequently misses capturing a given sinistral. Prey-handedness recognition should be advantageous for right-handed snail-eating snakes where frequently encountering sinistrals. Under dextral-predation by Pareas snakes, adaptive fixation of a prey population for a reversal gene instantaneously generates a sinistral species because interchiral mating is rarely possible. The novel warning, instead of sheltering, effect of sinistrality benefitting both predators and prey could further accelerate single-gene ecological speciation by left-right reversal.

SUBMITTER: Danaisawadi P

PROVIDER: S-EPMC4820687 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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A snail-eating snake recognizes prey handedness.

Danaisawadi Patchara P Asami Takahiro T Ota Hidetoshi H Sutcharit Chirasak C Panha Somsak S

Scientific reports 20160405

Specialized predator-prey interactions can be a driving force for their coevolution. Southeast Asian snail-eating snakes (Pareas) have more teeth on the right mandible and specialize in predation on the clockwise-coiled (dextral) majority in shelled snails by soft-body extraction. Snails have countered the snakes' dextral-predation by recurrent coil reversal, which generates diverse counterclockwise-coiled (sinistral) prey where Pareas snakes live. However, whether the snake predator in turn evo ...[more]

PMID: 27046345

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Project description:BackgroundEfficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as "goo-eating snakes". Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e.g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells.ResultsHere, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system.ConclusionsThe acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.

Project description:BackgroundAsymmetry in animal bodies and behavior has evolved several times, but our knowledge of their linkage is limited. Tanganyikan scale-eating cichlids have well-known antisymmetry in their bodies and behavior; individuals open their mouths leftward (righty) or rightward (lefty), and righties always attack the right flank of the prey, whereas lefties attack the left. This study analyzed the morphological asymmetry in a scale-eating characiform, Exodon paradoxus, and its behavioral handedness.Methodology/principal findingsEach eight E. paradoxus was observed for 1-h with a prey goldfish in an aquarium to detect the behavioral handedness. Following the experiment, the lateral differences in the mandibles and head-inclination of these eight and ten additional specimens were analyzed. Both measurements on the morphology showed a bimodal distribution, and the laterality identified by these two methods was always consistent within a given individual, indicating that the characin has morphological antisymmetry. Furthermore, this laterality significantly corresponded to behavioral handedness; that is, lefties more often rasped scales from the right flank of the prey and vice versa. However, the correlation between laterality and handedness is the opposite of that in the cichlids. This is due to differences in the feeding apparatus and technique. The characin has cuspids pointing forward on the external side of the premaxilla, and it thrusts its dominant body side outward from its body axis on the flank of the prey to tear off scales. By contrast, the cichlids draw their dominant body side inward toward the axis or rotate it to scrape or wrench off scales with the teeth lined in the opened mouth.Conclusions/significanceThis study demonstrated that the antisymmetry in external morphology and the corresponding behavioral handedness have evolved in two lineages of scale-eating fishes independently, and these fishes adopt different utilization of their body asymmetry to tear off scales.

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A snail-eating snake recognizes prey handedness.

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A snail-eating snake recognizes prey handedness.

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