Whole genome duplication is commonly believed to play key roles in vertebrate evolution. However, nowadays polyploidy exists in a few fish, amphibian, and reptile groups only, and seems to be an evolutionary dead-end in vertebrates. We investigate the evolutionary significance of polyploidization in Cyprinidae – a fish family that contains more polyploid species than any other vertebrate groups with integrating biogeographic, phylogenetic, and genomic analyses. First, polyploid species are found to be significantly frequent in higher altitude and lower mean annual temperature areas compared to diploid species in Cyprinidae. Second, a polyploidy-related diversification rate shift is observed in Cyprinidae. It is that increased net diversification rate is only seen in three polyploid lineages, and other polyploid lineages have similar net diversification rate as well as diploid lineages in Cyprinidae. Interestingly, significant ‘lag-times’ existed between polyploidization and radiation in Cyprinidae. Multiple polyploid lineages were established ~15 Mya through recurrent allopolyploidization events but net diversification rate did not start to increase until ~5 Mya – long after polyploidization events. Environmental changes associated with the continuous uplift of Tibetan Plateau and climate change have likely promoted the initial establishment and subsequent radiation of polyploidy in Cyprinidae. Finally, unique retention of duplicated genes in polyploid cyprinids adapted to harsh environments is found. Taken together, our results suggest that polyploidy in Cyprinidae is far more than an evolutionary dead-end, but rather shows substantially adaptive potential. Polyploid cyprinids thus constitute an ideal model system for unveiling largely unexplored consequences of whole genome duplication in vertebrates, from genomic evolution to species diversification.

Supplemental figures and tables