Rapid evolution of a coadapted gene complex: Evidence from the segregation Distorter (SD) system of meiotic drive in Drosophila melanogaster

Segregation Distorter (SD) is a system of meiotic drive found in natural populations of Drosophila melanogaster. Males heterozygous for an SD second chromosome and a normal homologue (SD+) produce predominantly SD- bearing sperm. The coadapted gene complex responsible for this transmission advantage spans the second chromosome centromere, consisting of three major and several minor interacting loci. To investigate the evolutionary history of this system, we surveyed levels of polymorphism and divergence at six genes that together encompass this pericentromeric region and span seven map units. Interestingly, there was no discernible divergence between SD and SD1 chromosomes for any of these molecular markers. Furthermore, SD chromosomes harbored much less polymorphism than did SD+ chromosomes. The results suggest that the SD system evolved recently, swept to appreciable frequencies worldwide, and carried with it the entire second chromosome centromeric region (roughly 10% of the genome). Despite its well-documented genetic complexity, this coadapted systems appears to have evolved on a time scale that is much shorter than can be gauge using nucleotide substitution data. Finally, the large genomic region hitchhiking with SD indicates that a multilocus, epistatically selected could affect the levels of DNA polymorphism observed in regions of reduced recombination.