Here we present a draft genome sequence of the nematode Pristionchus pacificus, a species that is associated with beetles and is used as a model system in evolutionary biology. With 169 Mb and 23,500 predicted protein-coding genes, the P. pacificus genome is larger than those of Caenorhabditis elegans and the human parasite Brugia malayi. Compared to C. elegans, the P. pacificus genome has more genes encoding cytochrome P450 enzymes, glucosyltransferases, sulfotransferases and ABC transporters, many of which were experimentally validated. The P. pacificus genome contains genes encoding cellulase and diapausin, and cellulase activity is found in P. pacificus secretions, indicating that cellulases can be found in nematodes beyond plant parasites. The relatively higher number of detoxification and degradation enzymes in P. pacificus is consistent with its necromenic lifestyle and might represent a preadaptation for parasitism. Thus, comparative genomics analysis of three ecologically distinct nematodes offers a unique opportunity to investigate the association between genome structure and lifestyle.

The widespread identification of genes without detectable homology in related taxa is a hallmark of genome sequencing projects in animals, together with the abundance of gene duplications. Such genes have been called novel, young, taxon-restricted, or orphans, but little is known about the mechanisms accounting for their origin, age, and mode of evolution. Phylogenomic studies relying on deep and systematic taxon sampling and using the comparative method can provide insight into the evolutionary dynamics acting on novel genes. We used a phylogenomic approach for the nematode model organism and sequenced six additional and two outgroup species. This resulted in 10 genomes with a ladder-like phylogeny, sequenced in one laboratory using the same platform and analyzed by the same bioinformatic procedures. Our analysis revealed that 68%-81% of genes are assignable to orthologous gene families, the majority of which defined nine age classes with presence/absence patterns that can be explained by single evolutionary events. Contrasting different age classes, we find that older age classes are concentrated at chromosome centers, whereas novel gene families preferentially arise at the periphery, are weakly expressed, evolve rapidly, and have a high propensity of being lost. Over time, they increase in expression and become more constrained. Thus, the detailed phylogenetic resolution allowed a comprehensive characterization of the evolutionary dynamics of genomes indicating that distribution of age classes and their associated differences shape chromosomal divergence. This study establishes the system for future research on the mechanisms that drive the formation of novel genes.

Cilia are complex organelles involved in sensory perception and motility with intraflagellar transport (IFT) proteins being essential for cilia assembly and function, but little is known about cilia in an evo‐devo context. For example, recent comparisons revealed conservation and divergence of IFT components in the regulation of social feeding behaviors between the nematodes Caenorhabditis elegans and Pristionchus pacificus. Here, we focus on the P. pacificus RFX transcription factor daf‐19, the master regulator of ciliogenesis in C. elegans. Two CRISPR/Cas9‐induced Ppa‐daf‐19 mutants lack ciliary structures in amphid neurons and display chemosensory defects. In contrast to IFT mutants, Ppa‐daf‐19 mutants do not exhibit social behavior. However, they show weak locomotive responses to shifts in oxygen concentration, suggesting partial impairment in sensing or responding to oxygen. To identify targets of Ppa‐daf‐19 regulation we compared the transcriptomes of Ppa‐daf‐19 and wild‐type animals and performed a bioinformatic search for the X‐box RFX binding‐site across the genome. The regulatory network of Ppa‐DAF‐19 involves IFT genes but also many taxonomically restricted genes. We identified a conserved X‐box motif as the putative binding site, which was validated for the Ppa‐dyf‐1 gene. Thus, Ppa‐DAF‐19 controls ciliogenesis, influences oxygen‐induced behaviors and displays a high turnover of its regulatory network.

Comparative studies have been of invaluable importance to the understanding of evolutionary biology. The evolution of developmental programs can be studied in nematodes at a single cell resolution given their fixed cell lineage. We have established Pristionchus pacificus as a major satellite organism for evolutionary developmental biology relative to Caenorhabditis elegans, the model nematode. Online genomic information to support studies in this satellite system can be accessed at . Our web resource offers diverse content covering genome browsing, genetic and physical maps, similarity searches, a community platform and assembly details. Content will be continuously improved as we annotate the P.pacificus genome, and will be an indispensable resource for P.pacificus genomics.

No abstract