Preferential Subfunctionalization of Slow-Evolving Genes after Allopolyploidization in Xenopus laevis

As paleopolyploid genomes evolve, the expression profiles of retained gene pairs are expected to diverge. To examine this divergence process on a large scale in a vertebrate system, we compare Xenopus laevis, which has retained ≈40% of loci in duplicate after a recent whole-genome duplication (WGD), with its unduplicated relative Silurana (Xenopus) tropicalis. This comparison of ingroup pairs to an outgroup allows the direction of change in expression profiles to be inferred for a set of 1,300 X. laevis pairs, relative to their single orthologs in S. tropicalis, across 11 tissues. We identify 68 pairs in which X. laevis is inferred to have undergone a significant reduction of expression in at least two tissues since WGD. Of these pairs, one-third show evidence of subfunctionalization, with decreases in the expression levels of different gene copies in two different tissues. Surprisingly, we find that genes with slow rates of evolution are particularly prone to subfunctionalization, even when the tendency for highly expressed genes to evolve slowly is controlled for. We interpret this result to be an effect of allopolyploidization. We then compare the outcomes of this WGD with an independent one that happened in the teleost fish lineage. We find that if a gene pair was retained in duplicate in X. laevis, the orthologous pair is more likely to have been retained in duplicate in zebrafish, suggesting that similar factors, among them subfunctionalization, determined which gene pairs survived in duplicate after the two WGDs.