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Abstract

The widespread identification of genes without detectable homology in related taxa is a hallmark of genome sequencing projects in animals. 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 the employment of the comparative method can provide insight into the evolutionary dynamics acting on novel genes. We used a phylogenomic approach for the nematode model organism Pristionchus pacificus and sequenced eight Pristionchus 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 novel gene families preferentially arise at chromosome arms, are typically lowly expressed and evolve rapidly. Over time they settle down at chromosome centers, increase expression, and become more constrained. However, younger gene families also show a higher propensity to being lost. Similarly, we performed epigenetic profiling in P. pacificus and analyzed orthologous, paralogous and novel genes using CHIP of seven histone modifications, ATAC seq, Iso-seq and RNA-seq. Consistent with previous findings we find that young genes are on average less expressed than older genes. Surprisingly however, the subset of orphan genes that are expressed exhibit distinct chromatin states from similarly expressed conserved genes. Orphan gene transcription is determined by a lack of repressive histone modifications, and transcriptional start sites that resemble enhancers defined by H3K4me1, H3K27ac and ATAC-seq peaks, in contrast to the strict correlation of conserved genes and promoters bearing H3K4me3 and H3K27ac. We also find that the majority of orphan genes are located on chromosome arms with repressive histone marks, yet expressed orphan genes are more randomly distributed. Our results support a model of new gene origination by rare integration into open chromatin near enhancers.