Cryptic asexual reproduction in Caenorhabditis nematodes revealed by interspecies hybridization

Abstract

Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction. AUTHOR SUMMARYEukaryotes employ two major reproductive strategies: sexual and asexual reproduction. Both types of reproduction have distinct theoretical costs and benefits, and most unicellular eukaryotes can switch between both modes. However, most multicellular eukaryotes are obligately sexual, implying that there are barriers to the evolution of asexuality from a sexual ancestor. Of the few asexual animal species, many are hybrids of two ancestral sexual species, suggesting that novel genetic interactions in hybrids facilitate the evolution of asexuality. One model suggests that genetic incompatibilities between divergent genomes in hybrids can modify female meiosis and paternal genome inheritance to facilitate asexual reproduction. While studying interspecies hybridizations of Caenorhabditis nematodes, we found that crossing two sexual species (C. nouraguensis and C. becei) disrupts female meiosis and paternal genome inheritance. Most offspring die during embryogenesis, but on rare occasions develop into viable and fertile adults that are produced asexually. This asexual reproduction involves the unusual production of eggs carrying two sets of maternal chromosomes and the loss of the paternal set of chromosomes. We hypothesize that genetic incompatibility between these two species disrupts maternal and paternal genome inheritance. This interspecies hybridization may serve as a model to study how genetic incompatibilities facilitate the emergence of asexuality.