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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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Related in: MedlinePlus

Shell-size-dependent associations of distributions between sinistral land snails and pareatids.Each bar indicates the proportion of genera composed of sinistral species in a 10-mm shell diameter interval ((a), flat snails; (b), tall snails; (c), total) showing the outcome of statistical analyses that used individual shell sizes as a numerical variable. Closed and open bars indicate the proportions within and outside the range of pareatid snakes, respectively. The number above each bar indicates the total number of genera included in each size range.
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f3: Shell-size-dependent associations of distributions between sinistral land snails and pareatids.Each bar indicates the proportion of genera composed of sinistral species in a 10-mm shell diameter interval ((a), flat snails; (b), tall snails; (c), total) showing the outcome of statistical analyses that used individual shell sizes as a numerical variable. Closed and open bars indicate the proportions within and outside the range of pareatid snakes, respectively. The number above each bar indicates the total number of genera included in each size range.

Mentions: We found that sinistral genera are marginally associated with snail-eating pareatid snakes in geographical distribution (Table 1; LRT for comparing GLMMs, d.f.=1, χ2=5.5, P=0.019). The statistical test incorporating distribution, shape and their interaction indicated that sinistral genera are more strongly associated with the sympatry with the snakes in flat snails than that in tall snails (LRT for comparing GLMMs, d.f.=1, χ2=9.8, P<0.01; Fig. 3a,b). The effect of interaction between distribution and size was also significant (LRT for comparing GLMMs, d.f.=1, χ2=8.6, P<0.01; Fig. 3c). Thus, the association of sinistral genera with the snakes is stronger in flat snails than in tall snails and larger snails. These findings cannot be explained by a phylogenetic artifact because the effect of higher taxa was statistically removed in every analysis by incorporating higher taxa (family) as a random effect (Fig. 4).


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)

Shell-size-dependent associations of distributions between sinistral land snails and pareatids.Each bar indicates the proportion of genera composed of sinistral species in a 10-mm shell diameter interval ((a), flat snails; (b), tall snails; (c), total) showing the outcome of statistical analyses that used individual shell sizes as a numerical variable. Closed and open bars indicate the proportions within and outside the range of pareatid snakes, respectively. The number above each bar indicates the total number of genera included in each size range.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Shell-size-dependent associations of distributions between sinistral land snails and pareatids.Each bar indicates the proportion of genera composed of sinistral species in a 10-mm shell diameter interval ((a), flat snails; (b), tall snails; (c), total) showing the outcome of statistical analyses that used individual shell sizes as a numerical variable. Closed and open bars indicate the proportions within and outside the range of pareatid snakes, respectively. The number above each bar indicates the total number of genera included in each size range.
Mentions: We found that sinistral genera are marginally associated with snail-eating pareatid snakes in geographical distribution (Table 1; LRT for comparing GLMMs, d.f.=1, χ2=5.5, P=0.019). The statistical test incorporating distribution, shape and their interaction indicated that sinistral genera are more strongly associated with the sympatry with the snakes in flat snails than that in tall snails (LRT for comparing GLMMs, d.f.=1, χ2=9.8, P<0.01; Fig. 3a,b). The effect of interaction between distribution and size was also significant (LRT for comparing GLMMs, d.f.=1, χ2=8.6, P<0.01; Fig. 3c). Thus, the association of sinistral genera with the snakes is stronger in flat snails than in tall snails and larger snails. These findings cannot be explained by a phylogenetic artifact because the effect of higher taxa was statistically removed in every analysis by incorporating higher taxa (family) as a random effect (Fig. 4).

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
Related in: MedlinePlus