Deciphering reticulate evolution of the largest group of polyploid vertebrates, the subfamily cyprininae (Teleostei: Cypriniformes)

Despite the rarity of polyploidy in animals, some groups with polyploid species exhibit complicated and interesting patterns of reticulate evolution. Here we focus on fishes in the subfamily Cyprininae, the largest polyploid group of vertebrates. The large number of polyploid taxa poses significant challenges for phylogenetic and evolutionary studies on this subfamily. In this study, we cloned and sequenced three single-copy nuclear loci to investigate the evolution of polyploidy in the Cyprininae. Topologies of nuclear gene trees were compared with a newly reconstructed mitochondrial tree. The data provided herein corroborate the hybrid origins of the tribes Torini, Cyprinini, Spinibarbini, Barbini, and also Probarbini. Based on results from this study and previous studies, we hypothesize that at least 13 independent polyploidization events have occurred during the evolution of the Cyprininae. We offer hypotheses on the origin of each polyploid group and show that a diploid group or the diploid ancestor of a polyploid group might have served as progenitor of one or two other polyploid groups. The evolutionary history of Cyprinine (since its first divergence) can be divided into three stages: the Diploid stage (69.2-43.4 Ma or million years ago), the Tetraploidization stage (43.4-18.9 Ma), and the Hexaploidization stage (18.9 Ma to present). The second stage is when all tetraploidization events happened, while the last stage is when all hexaploidization events and most genus- or species-specific polyploidization events occurred. The post-polyploidization dynamics of polyploid groups are complicated and warrant more genomic level studies. We showed that the subfamily Cyprininae may represent a more complicated polyploid system than most, if not all, other vertebrates and some plants, if one or more of the following factors are considered: number of polyploid species, number of different ploidy levels, and number and type of independent polyploidization events.

Automated summary

Despite the rarity of polyploidy in animals, the subfamily Cyprininae fishes present a complex and interesting pattern of reticulate evolution. Thirteen independent polyploidization events are hypothesized to have occurred during the evolution of Cyprininae, leading to a complicated post-polyploidization dynamics. The evolutionary history of Cyprinine can be divided into three stages, with the second stage witnessing all tetraploidization events and the last stage hosting hexaploidization events as well as species-specific polyploidization events.