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Detecting adaptive evolution based on association with ecological gradients: orientation matters!

ABSTRACT: Population genetic signatures of local adaptation are frequently investigated by identifying loci with allele frequencies that exhibit high correlation with ecological variables. One difficulty with this approach is that ecological associations might be confounded by geographic variation at selectively neutral loci. Here, we consider populations that underwent spatial expansion from their original range, and for which geographical variation of adaptive allele frequency coincides with habitat gradients. Using range expansion simulations, we asked whether our ability to detect genomic regions involved in adaptation could be impacted by the orientation of the ecological gradients. For three ecological association methods tested, we found, counter-intuitively, fewer false-positive associations when ecological gradients aligned along the main axis of expansion than when they aligned along any other direction. This result has important consequences for the analysis of genomic data under non-equilibrium population genetic models. Alignment of gradients with expansion axes is likely to be common in scenarios in which expanding species track their ecological niche during climate change while adapting to changing environments at their rear edge.

SUBMITTER: Frichot E

PROVIDER: S-EPMC4815498 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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Detecting adaptive evolution based on association with ecological gradients: orientation matters!

Frichot E E Schoville S D SD de Villemereuil P P Gaggiotti O E OE François O O

Heredity 20150218 1

Population genetic signatures of local adaptation are frequently investigated by identifying loci with allele frequencies that exhibit high correlation with ecological variables. One difficulty with this approach is that ecological associations might be confounded by geographic variation at selectively neutral loci. Here, we consider populations that underwent spatial expansion from their original range, and for which geographical variation of adaptive allele frequency coincides with habitat gra ...[more]

PMID: 25690180

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Project description:Deciphering the genomic variation that represents microevolutionary processes toward species divergence is key to understanding microbial speciation, which has long been under debate. Streptomycetes are filamentous bacteria that are ubiquitous in nature and the richest source of antibiotics; however, their speciation processes remain unknown. To tackle this issue, we performed a comprehensive population genomics analysis on Streptomyces albidoflavus residing in different habitats and with a worldwide distribution and identified and characterized the foundational changes within the species. We detected three well-defined phylogenomic clades, of which clades I and III mainly contained free-living (soil/marine) and insect-associated strains, respectively, and clade II had a mixed origin. By performing genome-wide association studies (GWAS), we identified a number of genetic variants associated with free-living or entomic (denoting or relating to insects) habitats in both the accessory and core genomes. These variants contributed collectively to the population structure and had annotated or confirmed functions that likely facilitate differential adaptation of the species. In addition, we detected higher levels of homologous recombination within each clade and in the free-living group than within the whole species and in the entomic group. A subset of the insect-associated strains (clade III) showed a relatively independent evolutionary trajectory with more symbiosis-favorable genes but little genetic interchange with the other lineages. Our results demonstrate that ecological adaptation promotes genetic differentiation in S. albidoflavus, suggesting a model of ecological speciation with gene flow in streptomycetes.IMPORTANCE Species are the fundamental units of ecology and evolution, and speciation leads to the astounding diversity of life on Earth. Studying speciation is thus of great significance to understand, protect, and exploit biodiversity, but it is a challenge in the microbial world. In this study, using population genomics, we placed Streptomyces albidoflavus strains in a spectrum of speciation and showed that the genetic differences between phylogenomic clusters evolved mainly by environmental selection and gene-specific sweeps. These findings highlight the role of ecology in structuring recombining bacterial species, making a step toward a deeper understanding of microbial speciation. Our results also raise concerns of an underrated microbial diversity at the intraspecies level, which can be utilized for mining of ecologically relevant natural products.

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Detecting adaptive evolution based on association with ecological gradients: orientation matters!

Publications

Detecting adaptive evolution based on association with ecological gradients: orientation matters!

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