Specific Interactions Between Autosome and Chromosomes Cause Hybrid Male Sterility in Species.

Hybrid male progeny from interspecies crosses are more prone to sterility or inviability than hybrid female progeny, and the male sterility and inviability often demonstrate parent-of-origin asymmetry. However, the underlying genetic mechanism of asymmetric sterility or inviability remains elusive. We previously established a genome-wide hybrid incompatibility (HI) landscape between and by phenotyping a large collection of strains each carrying a introgression. In this study, we systematically dissect the genetic mechanism of asymmetric sterility and inviability in both hybrid male and female progeny between the two species. Specifically, we performed reciprocal crosses between and different strains that each carry a GFP-labeled genomic fragment referred to as introgression, and scored the HI phenotypes in the F1 progeny. The aggregated introgressions cover 94.6% of the genome, including 100% of the chromosome. Surprisingly, we observed that two fragments that produce male sterility as an introgression rescued hybrid F1 sterility in males fathered by Subsequent backcrossing analyses indicated that a specific interaction between the -linked interaction and one autosome introgression is required to rescue the hybrid male sterility. In addition, we identified another two genomic intervals on chromosomes II and IV that can rescue the inviability, but not the sterility, of hybrid F1 males fathered by , suggesting the involvement of differential epistatic interactions in the asymmetric hybrid male fertility and inviability. Importantly, backcrossing of the rescued sterile males with led to the isolation of a 1.1-Mb genomic interval that specifically interacts with an -linked introgression, which is essential for hybrid male fertility. We further identified three genomic intervals on chromosome I, II, and III that produced inviability in all F1 progeny, dependent on or independent of the parent-of-origin. Taken together, we identified multiple independent interacting loci that are responsible for asymmetric hybrid male and female sterility, and inviability, which lays a foundation for their molecular characterization.