Abstract
Despite decades of work, our understanding of the distribution of fitness effects of segregating genetic variants in natural populations remains largely incomplete. One form of selection that can maintain genetic variation is spatially varying selection, such as that leading to latitudinal clines. While the introduction of population genomic approaches to understanding spatially varying selection has generated much excitement, little successful effort has been devoted to moving beyond genome scans for selection to experimental analysis of the relevant biology and the development of experimentally motivated hypotheses regarding the agents of selection; it remains an interesting question as to whether the vast majority of population genomic work will lead to satisfying biological insights. Here, motivated by population genomic results, we investigate how spatially varying selection in the genetic model system, Drosophila melanogaster, has led to genetic differences between populations in several components of the DNA damage response. UVB incidence, which is negatively correlated with latitude, is an important agent of DNA damage. We show that sensitivity of early embryos to UVB exposure is strongly correlated with latitude such that low latitude populations show much lower sensitivity to UVB. We then show that lines with lower embryo UVB sensitivity also exhibit increased capacity for repair of damaged sperm DNA by the oocyte. A comparison of the early embryo transcriptome in high and low latitude embryos provides evidence that one mechanism of adaptive DNA repair differences between populations is the greater abundance of DNA repair transcripts in the eggs of low latitude females. Finally, we use population genomic comparisons of high and low latitude samples to reveal evidence that multiple components of the DNA damage response and both coding and non-coding variation likely contribute to adaptive differences in DNA repair between populations.
Highlights
One of the promises of population genomic analyses is that, when combined with genome annotation, it can provide a rich source of hypotheses regarding the manifold ways in which selection may modify biological function
Motivated by population genomic evidence for spatially varying selection on DNA repair proteins in D. melanogaster [5], we focused on early embryo DNA damage response as a possible target of selection for three reasons
Control and UV-exposed treatments both show clines, for hatch rate, though with opposite sign slopes. While this is consistent with the idea that traits associated with decreased embryo UVB sensitivity are associated with reduced embryo viability in the absence of UVB exposure, alternative explanations are possible
Summary
One of the promises of population genomic analyses is that, when combined with genome annotation, it can provide a rich source of hypotheses regarding the manifold ways in which selection may modify biological function. Because these hypotheses are relatively agnostic with regard to our preconceived notions of the traits influenced by selection and their underlying genetics, such approaches may deepen and broaden our understanding of phenotypic evolution. Turner et al [5] reported that several genes associated with DNA repair harbored SNPs (single nucleotide polymorphisms) exhibiting high levels of differentiation between high and low latitude populations. We extend that observation in several new directions by integrating multiple data types to produce a portrait of the diverse molecular mechanisms associated with local adaptation in DNA repair, as well as identifying a likely ecological agent of selection
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