RNA-sequencing Analysis of Hybrid Females Reveals a Dominance of Expression of Alleles From Outcrossing Species Over Those From Selfing Species

The sister species Caenorhabditis briggsae and Caenorhabditis nigoni are the first Caenorhabditis nematode pair known to produce viable F1 hybrids, making them an ideal model for speciation study. Male F1 hybrids are lethal or sterile depending on the parent of origin, while F1 females, though viable, exhibit distinct phenotypes in fecundity and viability. Besides, both female hybrids could mate with C. nigoni males to produce viable progeny but experience hybrid breakdown when crossed with C. briggsae males. The molecular mechanisms driving these phenotype variations in F1 females remain unknown. Here, we analyzed the transcriptomes of F1 female hybrids from both crossing directions to examine whether a parent-specific haplotype dominates gene expression in the hybrids and to explore the mechanisms underlying the distinct phenotypes. We showed that in female hybrids from both directions, the C. nigoni haplotype was more abundantly expressed and main- tained the parental expression patterns better than that of C. briggsae. We also observed an upregulation of female-biased genes in the C. nigoni haplotype of F1 females, which may explain their compatibility with C. nigoni males for producing viable progeny, suggesting a haplotype-specific influence on female reproductive traits. Our mitochondrial gene analysis suggested a nuclear–cytoplasmic incompatibility marked by cis-dominated expression patterns of mitochondrial genes, which may contribute to the reduced viability in F1 females. This research provides insights into the expression pattern of interspecies F1 female hybrids and the mechanisms underlying nonlethal hybrid incompatibility defects.