Diverse genetic architectures on the Z chromosome underlie the two rules of speciation inPapiliobutterfly hybrids

AbstractTwo empirical rules arise from the incompatibility of interspecific hybrids: Haldane’s Rule predicts that the chromosomally heterogametic sex (XY or ZW) is more unfit after hybridization; the large-X/Z effect posits that sex chromosomes play a major role in incompatibility. Classical theories on these two rules rely on evidence mainly from taxa with male heterogamety, while female heterogamety received little investigation. Here, we reveal the genetic architectures of the two rules in hybrids between the butterfliesPapilio bianorandPapilio dehaanii, where the female is the heterogametic sex. In these crosses, hybrid females suffer from both body size abnormality and ovary dysgenesis, while males appear normal and fertile. Curiously, abnormal size in females is mapped to a continuum of Z-linked polygenes, each acting quantitatively with small phenotypic effects. This polygenic system, perhaps spanning the entire Z chromosome, also correctly predicts weaker incompatibility effects in males. For ovary dysgenesis, the underlying genetic architecture can be monogenic or polygenic with different maternal backgrounds. Most peculiarly, when comparing ovary dysgenesis in certain maternal backgrounds betweenPapilioandHeliconius, we find that F1recombination on the Z chromosome often rescues incompatibilities among backcross individuals, while a non-recombined Z chromosome almost always produces strong ovary defects regardless of ancestry. These results suggest that high fitness in these maternal backgrounds requires a balance between the total quantities of introgression on autosomes and the Z chromosome. Our study highlights that, in addition to incompatibility factors with large effects, genomically dispersed polygenes are also abundant in creating butterfly reproductive isolation.