Evidence of spatially varying selection acting on four chromatin-remodeling loci in Drosophila melanogaster

Abstract

The packaging of DNA into proper chromatin structure contributes to transcriptional regulation. This packaging is environment sensitive, yet its role in adaptation to novel environmental conditions is completely unknown. We set out to identify candidate chromatin-remodeling loci that are differentiated between tropical and temperate populations in Drosophila melanogaster, an ancestrally equatorial African species that has recently colonized temperate environments around the world. Here we describe sequence variation at seven such chromatin-remodeling loci, four of which (chd1, ssrp, chm, and glu) exhibit strong differentiation between tropical and temperate populations. An in-depth analysis of chm revealed sequence differentiation restricted to a small portion of the gene, as well as evidence of clinal variation along the east coasts of both the United States and Australia. The functions of chd1, chm, ssrp, and glu point to several novel hypotheses for the role of chromatin-based transcriptional regulation in adaptation to a novel environment. Specifically, both stress-induced transcription and developmental homeostasis emerge as potential functional targets of environment-dependent selection.

Figure 1.—

F_ST across a 35-kb region (D. melanogaster reference genome release 4.3) containing the chm locus. Each point corresponds to the midpoint of a single amplicon (see materials and methods) listed in supplemental Table S2, with the exception of peak seven, which corresponds to a mosaic of two amplicons. All genes located in this chromosomal region are indicated. The two significant replacement SNPs are in exon 1 (indicated with asterisks), although they occur in different amplicons. The serine/proline polymorphism occurs at peak five, while the arginine-proline amino acid polymorphism occurs at peak six.

Figure 2.—

Clinal variation at a differentiated SNP across latitudinal gradients in Australia (a) and the US (b), and equations for the regression lines.

Figure 3.—

Tajima's D across 35-kb region (D. melanogaster reference genome release 4.3) containing the chm locus in temperate and tropical Australia population samples. Each point corresponds to the midpoint of a single 1- to 1.3-kb amplicon.