Dataset Information

Rapid speciation with gene flow following the formation of Mt. Etna.

ABSTRACT: Environmental or geological changes can create new niches that drive ecological species divergence without the immediate cessation of gene flow. However, few such cases have been characterized. On a recently formed volcano, Mt. Etna, Senecio aethnensis and S. chrysanthemifolius inhabit contrasting environments of high and low altitude, respectively. They have very distinct phenotypes, despite hybridizing promiscuously, and thus may represent an important example of ecological speciation "in action," possibly as a response to the rapid geological changes that Mt. Etna has recently undergone. To elucidate the species' evolutionary history, and help establish the species as a study system for speciation genomics, we sequenced the transcriptomes of the two Etnean species, and the outgroup, S. vernalis, using Illumina sequencing. Despite the species' substantial phenotypic divergence, synonymous divergence between the high- and low-altitude species was low (dS = 0.016 ± 0.017 [SD]). A comparison of species divergence models with and without gene flow provided unequivocal support in favor of the former and demonstrated a recent time of species divergence (153,080 ya ± 11,470 [SE]) that coincides with the growth of Mt. Etna to the altitudes that separate the species today. Analysis of dN/dS revealed wide variation in selective constraint between genes, and evidence that highly expressed genes, more "multifunctional" genes, and those with more paralogs were under elevated purifying selection. Taken together, these results are consistent with a model of ecological speciation, potentially as a response to the emergence of a new, high-altitude niche as the volcano grew.

SUBMITTER: Osborne OG

PROVIDER: S-EPMC3787679 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Rapid speciation with gene flow following the formation of Mt. Etna.

Osborne Owen G OG Batstone Thomas E TE Hiscock Simon J SJ Filatov Dmitry A DA

Genome biology and evolution 20130101 9

Environmental or geological changes can create new niches that drive ecological species divergence without the immediate cessation of gene flow. However, few such cases have been characterized. On a recently formed volcano, Mt. Etna, Senecio aethnensis and S. chrysanthemifolius inhabit contrasting environments of high and low altitude, respectively. They have very distinct phenotypes, despite hybridizing promiscuously, and thus may represent an important example of ecological speciation "in acti ...[more]

PMID: 23973865

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Project description: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.

Dataset Information

Rapid speciation with gene flow following the formation of Mt. Etna.

Publications

Rapid speciation with gene flow following the formation of Mt. Etna.

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