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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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Survival advantage of sinistral snails.Each bar indicates the proportion of successful survival of sinistral S. perversa and dextral S. mercatoria (left), and of sinistral variant and dextral wild-type B. similaris (right) against predation by P. iwasakii (means across four snakes±s.e.; n=10 for each snake). S indicates attempts on sinistrals and D on dextrals.
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f2: Survival advantage of sinistral snails.Each bar indicates the proportion of successful survival of sinistral S. perversa and dextral S. mercatoria (left), and of sinistral variant and dextral wild-type B. similaris (right) against predation by P. iwasakii (means across four snakes±s.e.; n=10 for each snake). S indicates attempts on sinistrals and D on dextrals.

Mentions: In our experiments with dextral and sinistral Satsuma species, none of the dextral snails survived snake predation (Fig. 2; Supplementary Movie 1). In strong contrast, 87.5% of the sinistral snails survived predation (Supplementary Movie 2). The interaction effect of coiling direction and shell size on survival was significant (likelihood ratio test (LRT) for comparing generalized linear mixed models (GLMMs), d.f.=1, χ2=10.8, P<0.01; Fig. 2) when the effects of snake individual and snail groups were statistically removed in the combined data set including the results of the study by Hoso et al.22 This analysis, however, did not exclude the effects of interspecific differences in characteristics other than coiling direction, which potentially influence the survival rate. Throughout the experiment, snakes did not change the right-handed attacking behaviour. Snail extraction has commonly been observed in six other pareatid species (Aplopeltura boa, P. boulengeri, P. carinatus, P. formosensis, P. margaritophorus and P. stanleyi).


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)

Survival advantage of sinistral snails.Each bar indicates the proportion of successful survival of sinistral S. perversa and dextral S. mercatoria (left), and of sinistral variant and dextral wild-type B. similaris (right) against predation by P. iwasakii (means across four snakes±s.e.; n=10 for each snake). S indicates attempts on sinistrals and D on dextrals.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Survival advantage of sinistral snails.Each bar indicates the proportion of successful survival of sinistral S. perversa and dextral S. mercatoria (left), and of sinistral variant and dextral wild-type B. similaris (right) against predation by P. iwasakii (means across four snakes±s.e.; n=10 for each snake). S indicates attempts on sinistrals and D on dextrals.
Mentions: In our experiments with dextral and sinistral Satsuma species, none of the dextral snails survived snake predation (Fig. 2; Supplementary Movie 1). In strong contrast, 87.5% of the sinistral snails survived predation (Supplementary Movie 2). The interaction effect of coiling direction and shell size on survival was significant (likelihood ratio test (LRT) for comparing generalized linear mixed models (GLMMs), d.f.=1, χ2=10.8, P<0.01; Fig. 2) when the effects of snake individual and snail groups were statistically removed in the combined data set including the results of the study by Hoso et al.22 This analysis, however, did not exclude the effects of interspecific differences in characteristics other than coiling direction, which potentially influence the survival rate. Throughout the experiment, snakes did not change the right-handed attacking behaviour. Snail extraction has commonly been observed in six other pareatid species (Aplopeltura boa, P. boulengeri, P. carinatus, P. formosensis, P. margaritophorus and P. stanleyi).

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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