Six genome assemblies of Drosophila species for: Identification and genetic analysis of a pervasive "needle-eye" sperm phenotype in Drosophila sterile hybrid males

Interspecies hybrid sterility has been extensively studied, especially in the genus Drosophila. Hybrid sterility is more often found in the heterogametic (XX or ZW) sex, a trend called Haldane's rule. Although this phenomenon is pervasive, identification of a common genetic mechanism remains elusive, with modest support found for a range of potential theories. Here, we identify a single precise morphological phenotype, which we call "needle-eye sperm," that is associated with hybrid sterility in three separate species pairs that span the Drosophila genus. The nature of the phenotype indicates a common point of meiotic failure in sterile hybrid males. We used ten generations of backcross selection paired with whole-genome pooled sequencing to genetically map the regions underlying the needle-eye sperm phenotype. Surprisingly, the sterility phenotype was present in ~50% of males even after ten generations of backcrossing, yet the genetic map showed multiple regions associated with sterility, indicating multiple regions may have the capacity to be sufficient to induce sterility in the F1. Due to the common phenotype among sterile male hybrids and the strong effect of individual loci, further exploration of the genes uncovered here may identify a universal mechanism for the evolution of hybrid sterility.