Limits...
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.

Show MeSH
Distribution and phylogeny of the snail genus Satsuma.(a) Geographical distributions of sinistral (red) and dextral (blue) snails and pareatid snakes (orange) in East Asia. (b) Phylogenetic relationships of sinistral (red) and dextral (blue) snails based on maximum likelihood analysis of the combined CO1, ITS and ETS sequence data. Several clades containing only dextral species are compressed in blue (see Supplementary Fig. S1 for details). Specific names are listed in Supplementary Data 2. The numbers on branches indicate MP and ML bootstrap values, followed by Bayesian posterior probabilities (<50% not shown). Shells of some representative species are shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3105295&req=5

f5: Distribution and phylogeny of the snail genus Satsuma.(a) Geographical distributions of sinistral (red) and dextral (blue) snails and pareatid snakes (orange) in East Asia. (b) Phylogenetic relationships of sinistral (red) and dextral (blue) snails based on maximum likelihood analysis of the combined CO1, ITS and ETS sequence data. Several clades containing only dextral species are compressed in blue (see Supplementary Fig. S1 for details). Specific names are listed in Supplementary Data 2. The numbers on branches indicate MP and ML bootstrap values, followed by Bayesian posterior probabilities (<50% not shown). Shells of some representative species are shown.

Mentions: In our phylogenetic analyses of the snail genus Satsuma in Japan and Taiwan (Fig. 5a), the combined data matrix consisted of 2,842 nucleotide sites, of which 779 were parsimony informative. The maximum parsimony (MP) analysis resulted in the two most parsimonious trees (5,337 steps, consistency index excluding uninformative characters=0.2631, retention index=0.6068). The result of maximum likelihood (ML) and Bayesian analyses were largely consistent with the result of the MP analysis (Fig. 5b, Supplementary Fig. S1). In both the combined and separate data sets, the likelihood values of the constrained trees for sinistral lineage to be monophyletic were significantly lower than those of the unconstrained best trees (the approximately unbiased (AU) test2324, all P-values <0.01), indicating that the sinistral species have evolved from dextral ancestors multiple times within Satsuma.


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)

Distribution and phylogeny of the snail genus Satsuma.(a) Geographical distributions of sinistral (red) and dextral (blue) snails and pareatid snakes (orange) in East Asia. (b) Phylogenetic relationships of sinistral (red) and dextral (blue) snails based on maximum likelihood analysis of the combined CO1, ITS and ETS sequence data. Several clades containing only dextral species are compressed in blue (see Supplementary Fig. S1 for details). Specific names are listed in Supplementary Data 2. The numbers on branches indicate MP and ML bootstrap values, followed by Bayesian posterior probabilities (<50% not shown). Shells of some representative species are shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Distribution and phylogeny of the snail genus Satsuma.(a) Geographical distributions of sinistral (red) and dextral (blue) snails and pareatid snakes (orange) in East Asia. (b) Phylogenetic relationships of sinistral (red) and dextral (blue) snails based on maximum likelihood analysis of the combined CO1, ITS and ETS sequence data. Several clades containing only dextral species are compressed in blue (see Supplementary Fig. S1 for details). Specific names are listed in Supplementary Data 2. The numbers on branches indicate MP and ML bootstrap values, followed by Bayesian posterior probabilities (<50% not shown). Shells of some representative species are shown.
Mentions: In our phylogenetic analyses of the snail genus Satsuma in Japan and Taiwan (Fig. 5a), the combined data matrix consisted of 2,842 nucleotide sites, of which 779 were parsimony informative. The maximum parsimony (MP) analysis resulted in the two most parsimonious trees (5,337 steps, consistency index excluding uninformative characters=0.2631, retention index=0.6068). The result of maximum likelihood (ML) and Bayesian analyses were largely consistent with the result of the MP analysis (Fig. 5b, Supplementary Fig. S1). In both the combined and separate data sets, the likelihood values of the constrained trees for sinistral lineage to be monophyletic were significantly lower than those of the unconstrained best trees (the approximately unbiased (AU) test2324, all P-values <0.01), indicating that the sinistral species have evolved from dextral ancestors multiple times within Satsuma.

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