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Speciation and gene flow between snails of opposite chirality.

ABSTRACT: Left-right asymmetry in snails is intriguing because individuals of opposite chirality are either unable to mate or can only mate with difficulty, so could be reproductively isolated from each other. We have therefore investigated chiral evolution in the Japanese land snail genus Euhadra to understand whether changes in chirality have promoted speciation. In particular, we aimed to understand the effect of the maternal inheritance of chirality on reproductive isolation and gene flow. We found that the mitochondrial DNA phylogeny of Euhadra is consistent with a single, relatively ancient evolution of sinistral species and suggests either recent "single-gene speciation" or gene flow between chiral morphs that are unable to mate. To clarify the conditions under which new chiral morphs might evolve and whether single-gene speciation can occur, we developed a mathematical model that is relevant to any maternal-effect gene. The model shows that reproductive character displacement can promote the evolution of new chiral morphs, tending to counteract the positive frequency-dependent selection that would otherwise drive the more common chiral morph to fixation. This therefore suggests a general mechanism as to how chiral variation arises in snails. In populations that contain both chiral morphs, two different situations are then possible. In the first, gene flow is substantial between morphs even without interchiral mating, because of the maternal inheritance of chirality. In the second, reproductive isolation is possible but unstable, and will also lead to gene flow if intrachiral matings occasionally produce offspring with the opposite chirality. Together, the results imply that speciation by chiral reversal is only meaningful in the context of a complex biogeographical process, and so must usually involve other factors. In order to understand the roles of reproductive character displacement and gene flow in the chiral evolution of Euhadra, it will be necessary to investigate populations in which both chiral morphs coexist.

SUBMITTER: Davison A

PROVIDER: S-EPMC1182688 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The study of mechanisms that generate new species is considered fundamental for broad areas of ecology and evolution. Speciation is a continuous process in which reproductive isolation is established, and it is of fundamental importance to understand the origins of the adaptations that contribute to this process. Hybrid zones are considered natural laboratories for the study of speciation and represent ideal systems for such studies. Here, we investigated genomic differentiation between hybridizing Neotropical species Pitcairnia staminea (G. Lodd.) and P. albiflos (Herb.). Using thousands of SNPs genotyped through RAD-seq, we estimate effective population sizes, interspecific gene flow, as well as time of divergence between these two sister species and identify candidate genomic regions for positive selection that may be related to reproductive isolation. We selected different scenarios of speciation and tested them by using approximate Bayesian computation (ABC); we found evidence of divergence with gradual reduction in gene flow between these species over time, compatible with the hypothesis of speciation with gene flow between these Pitcairnia species. The parameter estimates obtained through ABC suggested that the effective population size of P. albiflos was around three times larger than that of P. staminea. Our divergence date estimates showed that these two species diverged during the Pliocene (4.7 Mya; CI = 1.3-8.5 Mya), which has likely allowed this species to accumulate genome-wide differences. We also detected a total of 17 of 4165 loci which showed signatures of selection with high genetic differentiation (F ST > 0.85), 12 of these loci were annotated in de novo assembled transcriptomes of both species, and 4 candidate genes were identified to be putatively involved in reproductive isolation. These four candidate genes were previously associated with the function of pollen development, pollen tube germination and orientation, abiotic stress, and flower scent in plants, suggesting an interplay between pre- and postpollination barriers in the evolution of reproductive isolation between such species.

Project description:Understanding why some groups of organisms are more diverse than others is a central goal in macroevolution. Evolvability, or the intrinsic capacity of lineages for evolutionary change, is thought to influence disparities in species diversity across taxa. Over macroevolutionary time scales, clades that exhibit high evolvability are expected to have higher speciation rates. Cone snails (family: Conidae, $>$900 spp.) provide a unique opportunity to test this prediction because their toxin genes can be used to characterize differences in evolvability between clades. Cone snails are carnivorous, use prey-specific venom (conotoxins) to capture prey, and the genes that encode venom are known and diversify through gene duplication. Theory predicts that higher gene diversity confers a greater potential to generate novel phenotypes for specialization and adaptation. Therefore, if conotoxin gene diversity gives rise to varying levels of evolvability, conotoxin gene diversity should be coupled with macroevolutionary speciation rates. We applied exon capture techniques to recover phylogenetic markers and conotoxin loci across 314 species, the largest venom discovery effort in a single study. We paired a reconstructed timetree using 12 fossil calibrations with species-specific estimates of conotoxin gene diversity and used trait-dependent diversification methods to test the impact of evolvability on diversification patterns. Surprisingly, we did not detect any signal for the relationship between conotoxin gene diversity and speciation rates, suggesting that venom evolution may not be the rate-limiting factor controlling diversification dynamics in Conidae. Comparative analyses showed some signal for the impact of diet and larval dispersal strategy on diversification patterns, though detection of a signal depended on the dataset and the method. If our results remain true with increased taxonomic sampling in future studies, they suggest that the rapid evolution of conid venom may cause other factors to become more critical to diversification, such as ecological opportunity or traits that promote isolation among lineages.

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Speciation and gene flow between snails of opposite chirality.

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