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The genomic basis of hybrid male sterility in Ficedula flycatchers

Identifying genes involved in genetic incompatibilities causing hybrid sterility or inviability is a long-standing challenge in speciation research, especially in studies based on natural hybrid zones. Here we present the first high-probability candidate genes for hybrid male sterility in birds by using a combination of whole genome sequence data, histology sections of testis and single cell transcriptomics of testis samples from male pied-, collared-, and hybrid flycatchers. We reveal failure of meiosis in hybrid males and propose candidate genes involved in genetic incompatibilities causing this failure. Based on identification of genes with non-synonymous fixed differences between the two species and revealing miss-expression patterns of these genes across the various stages of hybrid male spermatogenesis we conclude aberrant chromosome segregation and/or faulty chromatin packing. A lower proportion of spermatids produced by hybrid males implies that a proportion of the aberrant spermatids undergo apoptosis. Finally, we report an overrepresentation of Z-linkage of the revealed candidate incompatibility genes. Our results challenge the assumption that speciation processes are driven by fast evolving genes by showing that a few changes in genes with highly conserved and central functions may quickly ensure reproductive isolation through post-zygotic isolation.