Specific downregulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Abstract

Hybrid incompatibility (HI) prevents gene flow between species, thus lying at the heart of speciation genetics. One of the most common HIs is male sterility. Two superficially contradictory observations exist for hybrid male sterility. First, an introgression on the X chromosome is more likely to produce male sterility than on autosome (so-called large-X theory); second, spermatogenesis genes are enriched on the autosomes but depleted on the X chromosome (demasculization of X chromosome). Analysis of gene expression in Drosophila hybrids suggests a genetic interaction between X chromosome and autosomes that is essential for male fertility. However, the prevalence of such an interaction and its underlying mechanism remain largely unknown. Here we examine the interaction in nematode species by contrasting the expression of both coding genes and transposable elements (TEs) between hybrid sterile males and its parental nematode males. We use two lines of hybrid sterile males each carrying an independent introgression fragment from C. briggsae X chromosome in an otherwise C. nigoni background, which demonstrate similar defects in spermatogenesis. We observe a similar pattern of downregulated genes that are specific for spermatogenesis between the two hybrids. Importantly, the downregulated genes caused by the X chromosome introgressions show a significant enrichment on the autosomes, supporting an epistatic interaction between the X chromosome and autosomes. We investigate the underlying mechanism of the interaction by measuring small RNAs and find a subset of 22G RNAs specifically targeting the downregulated spermatogenesis genes are significantly upregulated in hybrids, suggesting that perturbation of small RNA-mediated regulation may contribute to the X-autosome interaction.