When genetic differences between populations disrupt the development of hybrid organisms, this prevents gene flow and enforces speciation. While prior studies have examined the genetic origins of hybrid incompatibility, the effects of incompatible factors on development remain poorly understood. Here, we investigate the mechanistic basis of hybrid incompatibility inCaenorhabditisnematodes by capitalizing on the ability ofC. brennerifemales to produce embryos after mating with males from several other species. These hybrids nearly always die, and their developmental problems begin immediately after fertilization, suggesting that post-fertilization barriers to hybridization originate from physical incompatibility between sperm and oocyte-derived factors rather than from zygotic transcription, which starts after the 4-cell stage. Sperm deliver chromatin, which expands to form a pronucleus, and a pair of centrioles, which form centrosomes that attach to the sperm-derived pronucleus and signal to establish the embryo's anterior-posterior axis. InC. brennerioocytes fertilized withC. eleganssperm, sperm-derived pronuclear expansion was delayed, frequent centrosome detachment was observed, and cortical polarity was disrupted. Live imaging revealed that defective polar body extrusion contributes to defects in mitotic spindle morphology. These early problems lead to abnormal embryonic organization in hybrids at the crucial 4-cell stage.C. brennerioocytes fertilized withC. remaneiorC. sp. 48sperm showed similar defects, and their severity and frequency increased with phylogenetic distance. Our results indicate that physical mismatches between sperm and oocyte-derived structures can destabilize development and may be a primary mechanism of hybrid incompatibility.
