Females and Males Contribute in Opposite Ways to the Evolution of Gene Order in Drosophila

An intriguing association between the spatial layout of chromosomes within nuclei and the evolution of chromosome gene order was recently uncovered. Chromosome regions with conserved gene order in the Drosophila genus are larger if they interact with the inner side of the nuclear envelope in D. melanogaster somatic cells. This observation opens a new door to understand the evolution of chromosomes in the light of the dynamics of the spatial layout of chromosomes and the way double-strand breaks are repaired in D. melanogaster germ lines. Chromosome regions at the nuclear periphery in somatic cell nuclei relocate to more internal locations of male germ line cell nuclei, which might prefer a gene order-preserving mechanism to repair double-strand breaks. Conversely, chromosome regions at the nuclear periphery in somatic cells keep their location in female germ line cell nuclei, which might be inaccessible for cellular machinery that causes gene order-disrupting chromosome rearrangements. Thus, the gene order stability for genome regions at the periphery of somatic cell nuclei might result from the active repair of double-strand breaks using conservative mechanisms in male germ line cells, and the passive inaccessibility for gene order-disrupting factors at the periphery of nuclei of female germ line cells. In the present article, I find evidence consistent with a DNA break repair-based differential contribution of both D. melanogaster germ lines to the stability/disruption of gene order. The importance of germ line differences for the layout of chromosomes and DNA break repair strategies with regard to other genomic patterns is briefly discussed.