Whole-Genome Analysis of Individual Meiotic Events in Drosophila melanogaster Reveals That Noncrossover Gene Conversions Are Insensitive to Interference and the Centromere Effect

Abstract

A century of genetic analysis has revealed that multiple mechanisms control the distribution of meiotic crossover events. In Drosophila melanogaster, two significant positional controls are interference and the strongly polar centromere effect. Here, we assess the factors controlling the distribution of crossovers (COs) and noncrossover gene conversions (NCOs) along all five major chromosome arms in 196 single meiotic divisions to generate a more detailed understanding of these controls on a genome-wide scale. Analyzing the outcomes of single meiotic events allows us to distinguish among different classes of meiotic recombination. In so doing, we identified 291 NCOs spread uniformly among the five major chromosome arms and 541 COs (including 52 double crossovers and one triple crossover). We find that unlike COs, NCOs are insensitive to the centromere effect and do not demonstrate interference. Although the positions of COs appear to be determined predominately by the long-range influences of interference and the centromere effect, each chromosome may display a different pattern of sensitivity to interference, suggesting that interference may not be a uniform global property. In addition, unbiased sequencing of a large number of individuals allows us to describe the formation of de novo copy number variants, the majority of which appear to be mediated by unequal crossing over between transposable elements. This work has multiple implications for our understanding of how meiotic recombination is regulated to ensure proper chromosome segregation and maintain genome stability.

The effects on neutral variability of recurrent selective sweeps and background selection

“…These values are consistent with the results of Miller et al (2016), and are similar to estimates from earlier studies of the rosy locus (Hilliker et al 1994). We did not vary the rate of initiation of gene conversion when using different rates of crossing over, since this rate appears to be fairly constant across the whole Drosophila genome (Comeron et al 2012;Miller et al 2016).…”

Estimating the parameters of background selection and selective sweeps in Drosophila in the presence of gene conversion

“…First, it seems likely that the relatively small values of the gene conversion parameters in ref. 23 are correct, rather than those of ref. 22, given their agreement with the classical results for the rosy locus (34,35) and their better fit to the data.…”

“…22 gave smaller estimates of the effect of BGS and larger γ estimates than when the lower value of ref. 23 was used (Figs. 3 and 4).…”

“…Using recent estimates of rates of crossing over and gene conversion for D. melanogaster (22,23), we found that the effects of BGS can account for only part of the observed relation between π S and K A , so that SSW effects need to be invoked. We estimated the average strength of selection on positively selected mutations, and the proportion of new mutations that are advantageous, for both NS and UTR sites.…”

Alfred Sturtevant Walks into a Bar: Gene Dosage, Gene Position, and Unequal Crossing Over in Drosophila

“…His findings are highly relevant to many areas of current study. Recent work has shown that unequal crossing over among repeats in tandem units analogous to Bar occurs de novo in about 1% of Drosophila meioses (Miller et al 2016a). This mechanism also underlies the expansion of gene families like Hox genes, key events in the evolution of different body plans (Holland 2015).…”