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Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow.

ABSTRACT: Theory predicts that speciation-with-gene-flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome-wide impacts of host-associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation-with-gene-flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co-occurring apple and hawthorn flies in nature. This striking genome-wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco-evolutionary dynamics and genome divergence.

SUBMITTER: Egan SP

PROVIDER: S-EPMC4744793 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow.

Egan Scott P SP Ragland Gregory J GJ Assour Lauren L Powell Thomas H Q THQ Hood Glen R GR Emrich Scott S Nosil Patrik P Feder Jeffrey L JL

Ecology letters 20150615 8

Theory predicts that speciation-with-gene-flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome-wide impacts of host-associated ...[more]

PMID: 26077935

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Project description:In bacteria, physiological change may be effected by a single gene acquisition, producing ecological differentiation without genetic isolation. Natural selection acting on such differences can reduce the frequency of genotypes that arise from recombination at these loci. However, gene acquisition can only account for recombination interference in the fraction of the genome that is tightly linked to the integration site. To identify additional loci that contribute to adaptive differences, we examined orthologous genes in species of Enterobacteriaceae to identify significant differences in the degree of codon selection. Significance was assessed using the Adaptive Codon Enrichment metric, which accounts for the variation in codon usage bias that is expected to arise from mutation and drift; large differences in codon usage bias were identified in more genes than would be expected to arise from stochastic processes alone. Genes in the same operon showed parallel differences in codon usage bias, suggesting that changes in the overall levels of gene expression led to changes in the degree of adaptive codon usage. Most significant differences between orthologous operons were found among those involved with specific environmental adaptations, whereas "housekeeping" genes rarely showed significant changes. When considered together, the loci experiencing significant changes in codon selection outnumber potentially adaptive gene acquisition events. The identity of genes under strong codon selection seems to be influenced by the habitat from which the bacteria were isolated. We propose a two-stage model for how adaptation to different selective regimes can drive bacterial speciation. Initially, gene acquisitions catalyze rapid ecological differentiation, which modifies the utilization of genes, thereby changing the strength of codon selection on them. Alleles develop fitness variation by substitution, producing recombination interference at these loci in addition to those flanking acquired genes, allowing sequences to diverge across the entire genome and establishing genetic isolation (i.e., protection from frequent homologous recombination).

Dataset Information

Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow.

Publications

Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow.

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