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A speciation gene for left-right reversal in snails results in anti-predator adaptation.

Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M - Nat Commun (2010)

Bottom Line: Worldwide biogeography reveals that stylommatophoran snail speciation by reversal has been accelerated in the range of pareatid snakes, especially in snails that gain stronger anti-snake defense and reproductive isolation from dextrals by sinistrality.Molecular phylogeny of Satsuma snails further provides intriguing evidence of repetitive speciation under snake predation.Our study demonstrates that a speciation gene can be fixed in populations by positive pleiotropic effects on survival.

View Article: PubMed Central - PubMed

Affiliation: Department of Community and Ecosystem Ecology, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan. hoso@m.tains.tohoku.ac.jp

ABSTRACT
How speciation genes can spread in a population is poorly understood. In land snails, a single gene for left-right reversal could be responsible for instant speciation, because dextral and sinistral snails have difficulty in mating. However, the traditional two-locus speciation model predicts that a mating disadvantage for the reversal should counteract this speciation. In this study, we show that specialized snake predation of the dextral majority drives prey speciation by reversal. Our experiments demonstrate that sinistral Satsuma snails (Stylommatophora: Camaenidae) survive predation by Pareas iwasakii (Colubroidea: Pareatidae). Worldwide biogeography reveals that stylommatophoran snail speciation by reversal has been accelerated in the range of pareatid snakes, especially in snails that gain stronger anti-snake defense and reproductive isolation from dextrals by sinistrality. Molecular phylogeny of Satsuma snails further provides intriguing evidence of repetitive speciation under snake predation. Our study demonstrates that a speciation gene can be fixed in populations by positive pleiotropic effects on survival.

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The snail-eating snake P. iwasakii.(a) Feeding behaviour of P. iwasakii. (b) A skull specimen (dorsal view) of P. iwasakii, exhibiting half a dozen more teeth on the right side of mandibles than on the left before hatching2255. Bars: 10 mm.
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f1: The snail-eating snake P. iwasakii.(a) Feeding behaviour of P. iwasakii. (b) A skull specimen (dorsal view) of P. iwasakii, exhibiting half a dozen more teeth on the right side of mandibles than on the left before hatching2255. Bars: 10 mm.

Mentions: Southeast Asian snakes in the family Pareatidae are regarded as dietary specialists of terrestrial snails and slugs21 (Fig. 1a). Because of the overwhelming predominance of dextral snails14, most pareatid snakes have evolved outstanding asymmetry in mandibular tooth number (Fig. 1b), which probably facilitates feeding on dextral snails22. The Japanese pareatid, P iwasakii, strikes an exposed soft part of a crawling snail from behind at a determined leftward angle to grasp the ventral shell surface with the upper jaw and the soft body by inserting the mandibles into the aperture. The snake then extracts the soft body by alternately protracting and retracting the asymmetric right and left mandibles (Supplementary Movie 1). Because of this 'right handedness' of sequential behaviour, the snake can rarely grasp a sinistral snail (Supplementary Movie 2). This survival advantage of sinistral variants may more than offset the mating disadvantage in dextral species and enhance the chance of population fixation for left–right reversal, which completes premating isolation22.


A speciation gene for left-right reversal in snails results in anti-predator adaptation.

Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M - Nat Commun (2010)

The snail-eating snake P. iwasakii.(a) Feeding behaviour of P. iwasakii. (b) A skull specimen (dorsal view) of P. iwasakii, exhibiting half a dozen more teeth on the right side of mandibles than on the left before hatching2255. Bars: 10 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105295&req=5

f1: The snail-eating snake P. iwasakii.(a) Feeding behaviour of P. iwasakii. (b) A skull specimen (dorsal view) of P. iwasakii, exhibiting half a dozen more teeth on the right side of mandibles than on the left before hatching2255. Bars: 10 mm.
Mentions: Southeast Asian snakes in the family Pareatidae are regarded as dietary specialists of terrestrial snails and slugs21 (Fig. 1a). Because of the overwhelming predominance of dextral snails14, most pareatid snakes have evolved outstanding asymmetry in mandibular tooth number (Fig. 1b), which probably facilitates feeding on dextral snails22. The Japanese pareatid, P iwasakii, strikes an exposed soft part of a crawling snail from behind at a determined leftward angle to grasp the ventral shell surface with the upper jaw and the soft body by inserting the mandibles into the aperture. The snake then extracts the soft body by alternately protracting and retracting the asymmetric right and left mandibles (Supplementary Movie 1). Because of this 'right handedness' of sequential behaviour, the snake can rarely grasp a sinistral snail (Supplementary Movie 2). This survival advantage of sinistral variants may more than offset the mating disadvantage in dextral species and enhance the chance of population fixation for left–right reversal, which completes premating isolation22.

Bottom Line: Worldwide biogeography reveals that stylommatophoran snail speciation by reversal has been accelerated in the range of pareatid snakes, especially in snails that gain stronger anti-snake defense and reproductive isolation from dextrals by sinistrality.Molecular phylogeny of Satsuma snails further provides intriguing evidence of repetitive speciation under snake predation.Our study demonstrates that a speciation gene can be fixed in populations by positive pleiotropic effects on survival.

View Article: PubMed Central - PubMed

Affiliation: Department of Community and Ecosystem Ecology, Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan. hoso@m.tains.tohoku.ac.jp

ABSTRACT
How speciation genes can spread in a population is poorly understood. In land snails, a single gene for left-right reversal could be responsible for instant speciation, because dextral and sinistral snails have difficulty in mating. However, the traditional two-locus speciation model predicts that a mating disadvantage for the reversal should counteract this speciation. In this study, we show that specialized snake predation of the dextral majority drives prey speciation by reversal. Our experiments demonstrate that sinistral Satsuma snails (Stylommatophora: Camaenidae) survive predation by Pareas iwasakii (Colubroidea: Pareatidae). Worldwide biogeography reveals that stylommatophoran snail speciation by reversal has been accelerated in the range of pareatid snakes, especially in snails that gain stronger anti-snake defense and reproductive isolation from dextrals by sinistrality. Molecular phylogeny of Satsuma snails further provides intriguing evidence of repetitive speciation under snake predation. Our study demonstrates that a speciation gene can be fixed in populations by positive pleiotropic effects on survival.

Show MeSH