Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Abstract

As a major origin of evolutionary novelties, gene duplication is a widespread phenomenon across species. However, the evolutionary force that determines the fate of duplicate genes is still under debate. Here, we studied the functional evolution of duplicate genes at both macroevolution and microevolution scales using the genomic sequences of eleven Caenorhabditis species and 773 C. elegans wild isolates. We found that compared to older duplicate genes and single-copy genes, recently duplicated gene copies showed rapid turnover, large genetic diversity, and signs of balancing and positive selection within the species. Young duplicate genes have low basal expression restricted to a few tissues but show highly responsive expression towards pathogenic infections. Recently duplicated genes are enriched in chemosensory perception, protein degradation, and innate immunity, implicating their functions in enhancing adaptability to external perturbations. Importantly, we found that young duplicate genes are rarely essential, while old duplicate genes have the same level of essentiality as singletons, suggesting that essentiality develops over a long time. Together, our work in C. elegans demonstrates that natural selection shapes the dynamic evolutionary trajectory of duplicate genes.

Transcript accumulation rates in the earlyCaenorhabditis elegansembryo

“…3E). We also find that clusters of high-rate genes (for example on chromosome II) belong to the same gene family, which likely also has risen out of duplication ( 48 ) (Fig. 4F).…”

“…C . Proportion of all high and low-rate genes that have duplications or are singletons (using data from Ma et al( 48 )). D .…”

“…Most of these clustered are either in the F-box family or the bath (BTB and MATH domain containing) family, both of which are substrate-binding adapters for ubiquitin-mediated proteolysis and are rapidly evolving in Caenorhabditis (47 ). More clusters of genes are seen on chromosome II compared to other chromosomes in several cell types, perhaps reflecting the large cluster of F-box genes that is enriched on this chromosome ( 48 ) (Supplementary Fig. 4).…”

“…Paralogous genes and embryonic lethal phenotypes. Data on gene duplications was obtained from Ma et al (48). A list of paralogs (Blast result from a e-value threshold of 10 −15 ) that were also syn-expressed was obtained from Tintori et al (18).…”

Transcript accumulation rates in the early Caenorhabditis elegans embryo

“…More clusters of genes are seen on chromosome II compared to other chromosomes in several cell types, perhaps reflecting the large cluster of F-box genes that is enriched on this chromosome (fig. S6, A to C) (56). When the F-box genes and those in the BTB, MATH, and SKR family involved in ubiquitin-mediated proteolysis are removed, the remaining high-rate genes are still enriched but not significantly on chromosome II, although a significant enrichment emerges on chromosome V (fig.…”