Multiple Pristionchus pacificus genomes reveal distinct evolutionary dynamics between de novo candidates and duplicated genes

The birth of new genes is a major molecular innovation driving phenotypic diversity across all domains of life. Although repurposing of existing protein-coding material by duplication is considered the main process of new gene formation, recent studies have discovered thousands of transcriptionally active sequences as a rich source of new genes. However, differential loss rates have to be assumed to reconcile the high birth rates of these incipient de novo genes with the dominance of ancient gene families in individual genomes. Here, we test this rapid turnover hypothesis in the context of the nematode model organism Pristionchus pacificus. We extended the existing species-level phylogenomic framework by sequencing the genomes of six divergent P. pacificus strains. We used these data to study the evolutionary dynamics of different age classes and categories of origin at a population level. Contrasting de novo candidates with new families that arose by duplication and divergence from known genes, we find that de novo candidates are typically shorter, show less expression, and are overrepresented on the sex chromosome. Although the contribution of de novo candidates increases toward young age classes, multiple comparisons within the same age class showed significantly higher attrition in de novo candidates than in known genes. Similarly, young genes remain under weak evolutionary constraints with de novo candidates representing the fastest evolving subcategory. Altogether, this study provides empirical evidence for the rapid turnover hypothesis and highlights the importance of the evolutionary timescale when quantifying the contribution of different mechanisms toward new gene formation.

Automated summary

The birth of new genes is a major driving force behind phenotypic diversity in all life forms. Previous studies have focused on the duplication of existing protein-coding material as the main process of new gene formation, but recent research has found that transcriptionally active sequences can also be a rich source of new genes. However, the high birth rates of these new genes have to be balanced with the loss rates in order to explain the dominance of ancient gene families in individual genomes. In this study, the researchers tested the hypothesis of rapid turnover in the nematode model organism Pristionchus pacificus. By sequencing the genomes of six divergent P. pacificus strains, they studied the evolutionary dynamics of different age classes and categories of origin at a population level. They found that de novo candidates, new genes that are not derived from duplication and divergence of known genes, are typically shorter, show less expression, and are overrepresented on the sex chromosome. In addition, the researchers discovered that de novo candidates have higher attrition rates compared to known genes within the same age class. These findings provide empirical evidence for the rapid turnover hypothesis and emphasize the importance of considering the evolutionary timescale when studying new gene formation.