Phylotranscriptomics of Pristionchus Nematodes Reveals Parallel Gene Loss in Six Hermaphroditic Lineages

Mutation and recombination are main drivers of phenotypic diversity, but the ability to create new allelic combinations is strongly dependent on the mode of reproduction. While most animals are dioecious (i.e., separated male and female sexes), in a number of evolutionary lineages females have gained the ability to self-fertilize [1, 2], with drastic consequences on effective recombination rate, genetic diversity, and the efficacy of selection [3]. In the genus Caenorhabditis, such hermaphroditic or androdioecious lineages, including C. briggsae and C. tropicalis, display a genome shrinkage relative to their dioecious sister species C. nigoni and C. brenneri, respectively [4, 5]. However, common consequences of reproductive modes on nematode genomes remain unknown, because most taxa contain single or few androdioecious species. One exception is the genus Pristionchus, with seven androdioecious species. Pristionchus worms are found in association with scarab beetles in worldwide samplings, resulting in deep taxon sampling and currently 39 culturable and available species. Here, we use phylotranscriptomics of all 39 Pristionchus species to provide a robust phylogeny based on an alignment of more than 2,000 orthologous clusters, which indicates that the seven androdioecious species represent six independent lineages. We show that gene loss is more prevalent in all hermaphroditic lineages than in dioecious relatives and that the majority of lost genes evolved recently in the Pristionchus genus. Further, we provide evidence that genes with male-biased expression are preferentially lost in hermaphroditic lineages. This supports a contribution of adaptive gene loss to shaping nematode genomes following the evolution of hermaphroditism. [Display omitted] •Phylotranscriptomics resolves the evolutionary history of Pristionchus nematodes•Hermaphroditsm arose at least six times independently within the genus•Gene loss in all hermaphroditic lineages is accelerated•Young and male-specific genes are preferentially lost While most animals have separated males and females, hermaphroditism evolved multiple times in different evolutionary lineages. Based on phylotranscriptomics of Pristionchus nematodes, Rödelsperger et al. show that the associated loss of male-biased genes, as found in Caenorhabditis, represents a general consequence of hermaphroditism.