Diversification and hybrid incompatibility in auto-pseudogamous species of Mesorhabditis nematodes

Pseudogamy is a reproductive system in which females rely on the sperm of males to activate their oocytes, generally parasitizing males of other species, but do not use the sperm DNA. The nematode Mesorhabditis belari uses a specific form of pseudogamy, where females produce their own males as a source of sperm. Males develop from rare eggs with true fertilization, while females arise by gynogenesis. Males thus do not contribute their genome to the female offspring. Here, we explored the diversity of reproductive mode within the Mesorhabditis genus and addressed species barriers in pseudogamous species.

To this end, we established a collection of over 60 Mesorhabditis strains from soil and rotting vegetal matter. We found that males from pseudogamous species displayed a reduced size of their body, male tail and sperm cells compared to males of sexual Mesorhabditis species, as expected for males that face little competition. Using rDNA sequences and crosses, we could define 11 auto-pseudogamous biological species, with closely related species pairs and a possible single origin of pseudogamy in the Mesorhabditis genus. Most crosses between males and females of different species did not even produce female progeny. This surprising species barrier in pseudogamous egg activation was pre or postcopulatory depending on the species pair. In the latter case, when hybrid embryos were produced, most arrested before the first embryonic cell division. Hybrid incompatibility between auto-pseudogamous species was due to defective interaction between sperm and oocyte as well as defective reconstitution of zygotic centrosomes.

We established a collection of sexual and pseudo-sexual species which offer an ideal framework to explore the origin and consequences of transition to asexuality. Our results demonstrate that speciation occurs in the pseudogamous state. Whereas genomic conflicts are responsible for hybrid incompatibility in sexual species, we here reveal that centrosomes constitute key organelles in the establishment of species barrier.