Polygenic Effects on the Z Chromosome Underlie Hybrid Incompatibility inPapilioandHeliconiusButterflies

Abstract The fitness of animal hybrids follows two empirical rules: hybrids of the heterogametic sex aremore unfit (Haldane’s Rule), and the sex chromosome is disproportionately involved in incompatibility (the large-X/Z effect). Whether these rules result from genetic mechanisms shared across taxa remains unknown, and existing explanations rarely consider female heterogametic taxa such as butterflies. Here, we investigate hybrid incompatibilities in Papilio and Heliconius butterflies, and show that defects coincide with unbalanced introgression between the Z chromosome and its genetic background. This polygenic mechanism predicts both rules because introgressed ancestry on the Z chromosome is more skewed in females, and is more variable than on all autosomes. Therefore, the explanation for both rules in butterflies shares little similarity with prevailing theories relying on dominance.