Molecular population genetics of Drosophila subtelomeric DNA

Abstract

DNA sequence surveys in yeast and humans suggest that the forces shaping telomeric polymorphism and divergence are distinctly more dynamic than those in the euchromatic, gene-rich regions of the chromosomes. However, the generality of this pattern across outbreeding, multicellular eukaryotes has not been determined. To characterize the structure and evolution of Drosophila telomeres, we collected and analyzed molecular population genetics data from the X chromosome subtelomere in 58 lines of North American Drosophila melanogaster and 29 lines of African D. melanogaster. We found that Drosophila subtelomeres exhibit high levels of both structural and substitutional polymorphism relative to linked euchromatic regions. We also observed strikingly different patterns of variation in the North American and African samples. Moreover, our analyses of the polymorphism data identify a localized hotspot of recombination in the most-distal portion of the X subtelomere. While the levels of polymorphism decline sharply and in parallel with rates of crossing over per physical length over the distal first euchromatic megabase pairs of the X chromosome, our data suggest that they rise again sharply in the subtelomeric region (approximately 80 kbp). These patterns of historical recombination and geographic differentiation indicate that, similar to yeast and humans, Drosophila subtelomeric DNA is evolving very differently from euchromatic DNA.

Figure 1.—

A typical Drosophila telomeric region. The left arrow points to the most terminal repeats (the transposable elements HeT-A and TART), while the right arrow points in the direction of the centromere. The subtelomere is composed of two main regions: the distal repetitive portion, or the TAS, and the centromere-proximal portion, labeled as the “chromosome-specific subtelomeric region.” Within this region, coding sequence is shaded, whereas repetitive sequence is depicted as diagonal stripes.

Figure 2.—

The subtelomeric region of the D. melanogaster X chromosome. Expected heterozygosity(π) in the 14 amplicons are reported above their corresponding locations on the chromosome. Significant positive values of Tajima's D are represented by a plus (+), while significant negative values are represented by a minus (−). Estimates for African (shading) and NA (solid) samples are reported separately. Annotated genes are shaded and labeled, and the TAS and the 1.688 satellite repeat sequence regions are shown in a striped pattern and labeled.

Figure 3.—

Crossover recombination density plot for both populations of D. melanogaster. Each square corresponds to a 1-kb window, beginning at the most-distal end of the X subtelomere. Blue squares correspond to regions with no data; yellow squares correspond to the highest density of crossover events; black corresponds to the lowest density of crossover events.

Figure 4.—

Crossover recombination density plot for the NA data. Each square corresponds to a 1-kb window, beginning at the most-distal end of the X subtelomere. Blue squares correspond to regions with no data; yellow squares correspond to the highest density of crossover events; black corresponds to the lowest density of crossover events.

Figure 5.—

SNP density plot using information from both populations of D. melanogaster. Each square corresponds to a 1-kb window, starting at the most-distal end of the X subtelomere. Yellow corresponds to the highest SNP density; black corresponds to the lowest SNP density.

Figure 6.—

Crossover recombination rates estimated using LDhat version 2.0. Log-transformed estimated rates are plotted along the X chromosome subtelomere. The distal-most region clearly shows an elevated level of recombination activity. In particular, the North American population possesses a distinguished crossover hotspot in the TAS region (to the left of position 10 kb). (a) Separate estimates for each of the NA and African data sets. (b) Estimates for the combined NA and African data.