The Paramecium aurelia complex is a group of 15 species so similar in morphologies that they were initially believed to be only one species. The sequencing of genomes from several species belonging to the P. aurelia complex has revealed that the members of the P. aurelia complex have diverged many million years ago, following a Whole-Genome Duplication (WGD) event that took place in the common ancestor of all P. aurelia lineages. WGDs have been rampant in the history of eukaryotes (yeast, plants, vertebrates, etc.) and it is well established that following a WGD, most pairs of duplicated genes eventually revert to a single copy state through pseudogenization. However, some pairs retain both duplicates for long evolutionary periods and it is still unclear why some duplicates are evolutionary successful while others are rapidly lost. Here, we analyzed genomics and transcriptomics data from three P. aurelia species and fond that dosage constraints are major factors opposing post-WGD gene loss in P. aurelia. We propose a model where a majority of WGD-derived duplicates preserve their ancestral function and are retained to produce enough of the proteins performing this same ancestral function. Under this model, the expression level of individual duplicated genes can evolve neutrally as long as they maintain a roughly constant summed expression, and this allows random genetic drift towards uneven contributions of the two copies to total expression. Our analysis suggests that once a high level of imbalance is reached, which can require substantial lengths of time, the copy with the lowest expression level contributes a small enough fraction of the total expression that selection no longer opposes its loss. Extension of our analysis to yeast species sharing a common ancestral WGD yields similar results, suggesting that duplicated-gene retention for dosage constraints followed by divergence in expression level and eventual deterministic gene loss might be a universal feature of post-WGD evolution. These results also illustrate the importance of using ciliates as a model organism for studying evolution following gene and genome duplications.