Caenorhabditis hybridizations reveal cytoplasmic-nuclear incompatibilities and asexual reproduction
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Lamelza, Piero
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Part 1: How species arise is a fundamental question in biology. Species can be defined as populations of interbreeding individuals that are reproductively isolated from other such populations. Therefore, understanding how reproductive barriers evolve between populations is essential for understanding the process of speciation. Hybrid incompatibility (for example, hybrid sterility or lethality) is a common and strong reproductive barrier in nature. Here we report a lethal incompatibility between two wild isolates, NIC59 and JU1825, of the nematode Caenorhabditis nouraguensis. Hybrid inviability results from the incompatibility between a maternally inherited cytoplasmic factor from each strain and a recessive nuclear locus from the other. Furthermore, cytoplasmic-nuclear incompatibility commonly occurs between other wild isolates, indicating that this is a significant reproductive barrier within C. nouraguensis. We hypothesize that the maternally inherited cytoplasmic factor is the mitochondrial genome and that mitochondrial dysfunction underlies hybrid death. We find that the JU1825 nuclear incompatibility locus maps to chromosome III and the NIC59 nuclear incompatibility locus maps to chromosome IV, indicating the incompatibilities are genetically distinct. We have finely mapped the JU1825 nuclear incompatibility locus to a 100 kb region containing tandem and diversified repeats of F-box domain, transmembrane domain and nuclear hormone receptors genes. There are also exact tandem repeats of a leucine-tRNA. The NIC59 and JU1825 mitochondrial genomes differ by 95 SNPs and 1 bp indel. Potential functional differences between the genomes include single non-synonymous changes in nd-1 and cox-1 (components of complex I and IV of the electron transport chain, respectively), a SNP in the cysteine tRNA and 3 SNPs and 1 bp indel in the 16s rRNA. This system has the potential to shed light on the dynamics of divergent mitochondrial-nuclear coevolution and its role in promoting speciation. Part 2: Most animal species reproduce by sex. Theory predicts there are advantages to being able to switch reproduction between sexual and asexual modes. However, facultative sex is rarely observed in animals, implying that there are strong selective pressures that prevent asexuality arising from an obligately sexual ancestor. One of the critical steps in the evolution of asexuality from a sexual ancestor is the transition from haploid to diploid maternal inheritance. Here we report that interspecific hybridization between two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) results in two classes of viable offspring. The first class consists of fertile offspring, which 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. The second class consists of sterile hybrid offspring, which inherit both a diploid maternal genome and a haploid paternal genome. Using whole-genome sequencing of individual viable worms, we show that diploid maternal inheritance in both asexually produced and hybrid offspring results from the inheritance of two randomly selected homologous chromatids from C. nouraguensis oocytes. This genetic mechanism of diploid maternal inheritance is indistinguishable from that of many obligately asexual species. Furthermore, we show that intraspecies C. nouraguensis crosses can also result in a low frequency of asexual reproduction through diploid maternal inheritance. Thus, C. nouraguensis provides a genetically tractable model to study the evolutionary origins of asexuality from obligately sexual species.