The architecture of both phenotypic variation and reproductive isolation are important problems in evolutionary genetics. The nematode genus Caenorhabditis includes both gonochoristic (male/female) and androdioecious (male/hermaprodite) species. However, the natural genetic variants distinguishing reproductive mode remain unknown, and nothing is known about the genetic basis of postzygotic isolation in the genus. Here we describe the hybrid genetics of the first Caenorhabditis species pair capable of producing fertile hybrid progeny, the gonochoristic Caenorhabditis sp. 9 and the androdioecious C. briggsae. Though many interspecies F 1 arrest during embryogenesis, a viable subset develops into fertile females and sterile males. Reciprocal parental crosses reveal asymmetry in male-specific viability, female fertility, and backcross viability. Selfing and spermatogenesis are extremely rare in XX F 1 , and almost all hybrid self-progeny are inviable. Consistent with this, F 1 females do not express male-specific molecular germline markers. We also investigated three approaches to producing hybrid hermaphrodites. A dominant mutagenesis screen for self-fertile F 1 hybrids was unsuccessful. Polyploid F 1 hybrids with increased C. briggsae genomic material did show elevated rates of selfing, but selfed progeny were mostly inviable. Finally, the use of backcrosses to render the hybrid genome partial homozygous for C. briggsae alleles did not increase the incidence of selfing or spermatogenesis relative to the F 1 generation. These hybrid animals were genotyped at 23 loci, and significant segregation distortion (biased against C. briggsae) was detected at 13 loci. This, combined with an absence of productive hybrid selfing, prevents formulation of simple hypotheses about the genetic architecture of hermaphroditism. In the near future, this hybrid system will likely be fruitful for understanding the genetics of reproductive isolation in Caenorhabditis.

A ‘sibling’ species of the model organism Caenorhabditis elegans has long been sought for use in comparative analyses that would enable deep evolutionary interpretations of biological phenomena. Here, we describe the first sibling species of C. elegans, C. inopinata n. sp., isolated from fig syconia in Okinawa, Japan. We investigate the morphology, developmental processes and behaviour of C. inopinata, which differ significantly from those of C. elegans. The 123-Mb C. inopinata genome was sequenced and assembled into six nuclear chromosomes, allowing delineation of Caenorhabditis genome evolution and revealing unique characteristics, such as highly expanded transposable elements that might have contributed to the genome evolution of C. inopinata. In addition, C. inopinata exhibits massive gene losses in chemoreceptor gene families, which could be correlated with its limited habitat area. We have developed genetic and molecular techniques for C. inopinata; thus C. inopinata provides an exciting new platform for comparative evolutionary studies.

Summary Evolutionary transitions between sexual modes could be potent forces in genome evolution. Several Caenorhabditis nematode species have evolved self-fertile hermaphrodites from the obligately outcrossing females of their ancestors. We explored the relationship between sexual mode and global gene expression by comparing two selfing species, C. elegans and C. briggsae, with three phylogenetically informative outcrossing relatives, C. japonica, C. brenneri, and C. japonica. Adult transcriptome assemblies from the selfing species are consistently and strikingly smaller than those of the outcrossing species. Against this background of overall simplification, genes conserved in multiple outcrossing species with strong sex-biased expression are even more likely to be missing from the genomes of the selfing species. In addition, the sexual regulation of remaining transcripts has diverged markedly from the ancestral pattern in both selfing lineages, though in distinct ways. Thus, both the complexity and the sexual specialization of transciptomes are rapidly altered in response to the evolution of self-fertility. These changes may result from the combination of relaxed sexual selection and a recently reported genetic mechanism favoring genome shrinkage in partial selfers.

Sperm from other species invade female tissues to cause sterility and death, helping to keep nematode species boundaries intact.