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.
Highlights
Sex is the most common form of reproduction in multicellular eukaryotes
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
Summary
Sex is the most common form of reproduction in multicellular eukaryotes. Diploid females and males generate haploid eggs and sperm that fuse to produce diploid offspring. Despite the predicted advantages of sex, it has theoretical costs, such as the need to find a mate and the production of offspring that inherit only half of an individual’s genome [2,3]. Females of asexual species independently generate their own offspring and pass on their entire genome. Because obligate sex is the predominant form of reproduction in multicellular organisms [6], it is likely there are strong barriers that prevent the origin of asexuality from a sexual ancestor or its persistence [7]. By studying rare cases of asexual animal species, we can better understand the circumstances that facilitate the evolution of asexual reproduction
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