Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Abstract

The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints. Whole-genome duplications are a powerful evolutionary force, and much interest is focused on what happens to genes duplicated in these events. The genome of the ciliate Paramecium tetraurelia has now been sequenced, and its nearly 40,000 genes (it's a very 'gene rich' genome) show evidence of at least three whole-genome duplications. As the gene order is particularly well conserved in Paramecium, it is possible to identify genes that duplicated at each event, providing a complete picture of gene loss at different time points after duplications. A study of the duplicated genes in Paramecium tetraurelia suggests that after whole-genome duplication events, many duplicated genes are not able to immediately functionally diverge, because dosage constraints act on them. These dosage constraints also prevent loss of many duplicated genes after whole genome duplications.