Comparative analysis of gene duplications and their impact on expression levels in nematode genomes

Abstract

Gene duplication is a major mechanism that plays a vital role in different evolutionary innovations, ranging from generating novel traits to phenotypic plasticity. Evolutionary impact of gene duplication and the fate of duplicated genes has been studied in detail. However, little is known about the impact of gene duplication on gene expression with respect to different evolutionary time scales. Here, we study genome-wide patterns of gene duplications in nematodes and assess their effect on expression levels. This study encompasses various macroevolutionary comparisons at different time scales and microevolutionary comparisons within the species Pristionchus pacificus. At the macroevolutionary level, by comparing species separated more than 280 million years ago, we found various lineage-specific expansions in multiple gene families along the Pristionchus lineage. Moreover, we found that duplicated genes are highly enriched among developmentally regulated genes. Interestingly, the results also show evidence for selection on duplication to increases the gene expression levels in a developmental stage-specific manner. To gain insights into the microevolution of gene expression levels after gene duplication, we compared different strains of P.pacificus and found that an additional gene copy does usually not increase gene expression levels in the different strains. Furthermore, we found a strong depletion of duplicated genes in large parts of the P. pacificus genome indicating towards negative selection against gene duplication. This shows that the impact on gene expression levels following gene duplication differs dramatically, where a selection for increased gene dosage dominates macroevolution and negative selection on gene duplication dominates within species level. This led us to wonder what happens at the intermediate time scale. We compared recent duplicates of P. pacificus with their single-copy orthologs in two closely related species and found a pattern similar to the microevolutionary trend. Additionally, comparison of closely related species of the Strongyloides genus and its developmental transcriptome also shows overall strong depletion of duplicated genes, similar to the observation at the microevolutionary level. At the same time, a strong enrichment of duplicated genes was found at a developmental stage associated with the parasitic activity of the nematodes. Similar to the macroevolutionary picture of P. pacificus, we also found selection for higher gene dosage in parasitism-associated gene families of S. papillosus, indicating the adaptive potential of duplicated genes. Even though these studies show widespread selection against both duplication and changes in gene expression, duplications are favoured in some conditions leading to adaptive changes in the organism. Overall this indicates that the regulation of expression levels of duplicated genes was subjected to different selection processes at different time scales, which represent a complex interplay between different evolutionary processes like natural selection, population dynamics, and genetic drift.