Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly

Abstract

Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (M^V) has two intact Mdmd copies in a palindrome. M on chromosome III (M^III) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (M^II) and the Y (M^Y) share M^III-like architecture, but with fewer repeats. M^Y additionally shares M^V-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from M^III and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.

For sexually reproducing organisms, experimental models to study the evolution of primary sex-determining loci are scarce. This study shows male-determining loci on  proto-Y chromosomes of the housefly, containing the same gene, can genomically diverge into regions of various complexity.