Fine-Scale Heterogeneity in Crossover Rate in thegarnet-scallopedRegion of theDrosophila melanogasterX Chromosome

Abstract

Homologous recombination affects myriad aspects of genome evolution, from standing levels of nucleotide diversity to the efficacy of natural selection. Rates of crossing over show marked variability at all scales surveyed, including species-, population-, and individual-level differences. Even within genomes, crossovers are nonrandomly distributed in a wide diversity of taxa. Although intraand intergenomic heterogeneities in crossover distribution have been documented in Drosophila, the scale and degree of crossover rate heterogeneity remain unclear. In addition, the genetic features mediating this heterogeneity are unknown. Here we quantify finescale heterogeneity in crossover distribution in a 2.1-Mb region of the Drosophila melanogaster X chromosome by localizing crossover breakpoints in 2500 individuals, each containing a single crossover in this specific X chromosome region. We show 90-fold variation in rates of crossing over at a 5-kb scale, place this variation in the context of several aspects of genome evolution, and identify several genetic features associated with crossover rates. Our results shed new light on the scale and magnitude of crossover rate heterogeneity in D. melanogaster and highlight potential features mediating this heterogeneity.

Background selection as baseline for nucleotide variation across theDrosophilagenome

“…Second, recent wholegenome studies of recombination rates in D. melanogaster exposed extensive heterogeneity in the distribution of crossover rates even after removing sub-telomeric and centromeric regions [31]. This high degree of variation in recombination rates across D. melanogaster chromosomes is observed when recombination is obtained from a single cross of two specific strains [31,32] as well as when analyzing a species' average obtained from combining genetic maps from crosses of several natural strains [31]. The presence of coldspots of recombination embedded in chromosomal regions assumed to have high recombination rates, therefore, provides the opportunity for BGS to play a more significant role across broader genomic regions than previously anticipated [31].…”

Studying Recombination with High-Throughput Sequencing: An Educational Primer for Use with “Fine-Scale Heterogeneity in Crossover Rate in the garnet-scalloped Region of the Drosophila melanogaster X chromosome”

“…grandparent vs. the g sd grandparent were observed and used the "allele frequency" approach described above to infer how much recombination occurred between each pair of adjacent markers. Moving from left to right across Figure 3b in Singh et al (2013) shows that more of the offspring had the allele derived from the g-sd grandparent's allele, analogous to the transition from 1/5 at marker 2 to 4/5 at marker 3 in our fictitious example discussed above and in Figure 2. This procedure was done separately for the + sd recombinants and the g + recombinants, as depicted in Singh et al's Figure 3b vs. Figure 3a (Singh et al 2013), respectively, and the patterns are opposite of each other, as expected.…”

“…One of the coolest things about the study by Singh et al (2013) is that the authors use a classical Drosophila genetics technique dating back over 100 years. In the early 1900s, Thomas Hunt Morgan, a fly geneticist at Columbia University, discovered sex chromosome inheritance using several mutations on the X chromosome (Morgan 1910).…”

“…The project by Singh et al (2013) has one facet that is simpler than the example above and two facets that are more challenging. The simpler facet is that they already have an assembled D. melanogaster sequence with which to work (Adams et al 2000).…”

“…Failure of this process can result in an egg or sperm having too many or too few chromosomes, which is fatal or severely developmentally debilitating. Singh et al (2013) explore differences in the frequency of recombination events across part of the Drosophila melanogaster genome. As they discuss, researchers have found that recombination events do not happen randomly across the genome in most organisms studied.…”