The evolutionary consequences of whole-genome duplication in Paramecium

Whole-genome duplications (WGDs) are widespread among eukaryotic lineages and have been identified in the ancestry of many model systems. Despite this prevalence, the evolutionary ramifications of WGD remain poorly understood. The Paramecium aurelia complex is a group of 15 species that are highly similar morphologically and ecologically. At least 3 WGDs have been identified in the ancestry of this lineage. In this work, we present the macronuclear genome sequences of P. biaurelia and sexaurelia and compare them to the published sequence of tetraurelia. We also present the sequence of an outgroup species, Paramecium caudatum, which diverged before the two most recent WGDs. We use these four species to analyze patterns of duplicate gene retention and loss over three WGDs of varying ages. We demonstrate that GC content, expression level, and functional category of ancestral, pre-duplication genes correlate with duplicate-gene retention across multiple WGDs. In addition, we find that gene conversion acts to significantly homogenize duplicates from the recent WGD but does not appear to currently have a significant affect on duplicates from the intermediate WGD. Finally, we show that the speciation events in the aurelia lineage are reinforced by divergent resolution of duplicate genes. Though the rate of divergent resolution declines over time, some divergent resolutions can occur long after a WGD, indicating that reinforcement of reproductive isolation via this mechanism may continue for a significant period of time following a whole-genome duplication event.