| Summary: | <p>The genetic mechanisms by which natural populations maintain abundant phenotypic variation and adapt to their local environments remains a controversial topic in evolutionary biology. An intriguing mechanism involving highly mutable microsatellites follows the tuning knob model which proposes that stepwise changes in microsatellite allele lengths reciprocally generate phenotypic variation in a stepwise manner. In this study, I explored the predictions of the tuning knob model focusing specifically on transcribed microsatellites within and among natural populations of common sunflower (<i>Helianthus annuus</i> L.) transecting a latitudinal cline. An RNA-Seq experiment was conducted on 95 individuals from Kansas and Oklahoma grown in a common garden. To explore the potential role that microsatellites play in gene expression divergence in common sunflower, enrichment of microsatellites within differentially expressed (DE) genes was assessed. The results showed that A and AG repeat-containing microsatellites are enriched within DE genes and that 83.5% of these microsatellites are located within untranslated regions (UTRs). This finding is consistent with a role for transcribed microsatellites in gene expression divergence. RNA-Seq data were then used to assess microsatellite allele length effects on gene expression. Of all the microsatellites characterized in a reference transcriptome, 3,325 were consistently genotyped. The study identified 479 microsatellites at which allele length significantly correlated with gene expression (eSTRs). When irregular allele sizes were removed from the analysis, the number of eSTRs rose to 2379. eSTRs were most abundant within UTRs (70.4%) which suggests that they are well-positioned as cis-regulatory elements. A population genetic study conducted with 672 individuals across 17 sunflower populations from Saskatchewan to Oklahoma revealed strong signatures of directional selection acting on 13 eSTRs compared to 19 anonymous microsatellites assumed to evolve in a neutral fashion. This demonstrates that longer or shorter alleles may be favored in more extreme environments to that considered in the focal study. A second common garden experiment conducted with populations further north and south of focal populations revealed consistent patterns of correlation between microsatellite allele length and gene expression at some eSTRs. This study provides evidence that a substantial number of transcribed microsatellites function as tuning knobs of adaptation in common sunflower by modulating gene expression in a stepwise manner. These findings imply that the genomes of natural populations may include hundreds of active tuning knobs that can facilitate rapid evolution.</p>
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