The order Acipenseriformes, which includes sturgeons and paddlefishes, represents “living fossils” with complex genomes that are good models for understanding whole-genome duplication (WGD) and ploidy evolution in fishes. Here, we sequenced and assembled the first high-quality chromosome-level genome for the complex octoploid Acipenser sinensis (Chinese sturgeon), a critically endangered species that also represents a poorly understood ploidy group in Acipenseriformes. Our results show that A. sinensis is a complex autooctoploid species containing four kinds of octovalents (8n), a hexavalent (6n), two tetravalents (4n), and a divalent (2n). An analysis taking into account delayed rediploidization reveals that the octoploid genome composition of Chinese sturgeon results from two rounds of homologous WGDs, and further provides insights into the timing of its ploidy evolution. This study provides the first octoploid genome resource of Acipenseriformes for understanding ploidy compositions and evolutionary trajectories of polyploidy fishes.

Some East Asian rivers experienced repeated rearrangements due to Indian–Asian Plates’ collisions and an uplift of the Tibetan Plateau. For the upper Changjiang (Yangtze/Jinsha River), its ancient south-flowing course and subsequent capture by the middle Changjiang at the First Bend (FB) remained controversial. The DNA of freshwater fishes possess novel evolutionary signals of these tectonic events. In this study, mtDNA Cyt b sequences of endemic Schizopygopsis fish belonging to a highly specialized grade of the Schizothoracinae from the eastern Tibetan Plateau were used to infer the palaeo-drainages connectivity history of the upper Changjiang system. Through phylogenetic reconstruction, a new clade D of Schizopygopsis with three genetic clusters and subclusters (DI, DII, DIIIa, and DIIIb) were identified from the upper Yalong, Changjiang, and Yellow Rivers; the Shuiluo River; the FB-upper Changjiang; and the Litang River; respectively. Ancient drainage connections and capture signals were indicated based on these cladogenesis events and ancestral origin inference: (1) the upper Yalong River likely acted as a dispersal origin of Schizopygopsis fish to the adjacent upper Yellow and Changjiang Rivers at ca. 0.34 Ma; (2) the Litang River seemed to have directly drained into the upper Changjiang/Yangtze/Jinsha River before its capture by the Yalong River at ca. 0.90 Ma; (3) the Shuiluo River likely flowed south along a course parallel to the upper Changjiang before their connection through Hutiao Gorge; (4) a palaeo-lake across the contemporary Shuiluo, Litang, and Yalong Rivers was inferred to have served as an ancestral origin of clade D of Schizopygopsis at 1.56 Ma. Therefore, this study sheds light on disentangling ambiguous palaeo-drainage history through integrating biological and geological evidence.

The Order Acipenseriformes, which include sturgeons and paddlefishes, represent “living fossils” with complex genomes that are good models for understanding whole genome duplication (WGD) and ploidy evolution in fishes. Here we sequenced and assembled the first high-quality chromosome-level genome for the complex octoploid Acipenser sinensis (Chinese sturgeon), a critically endangered species that also represents a poorly understood ploidy group in Acipenseriformes. Our results show that A. sinensis is a complex autooctoploid species containing four kinds of octovalents (8 n), a hexavalent (6 n), two tetravalents (4 n), and a divalent (2 n). We propose based on an analysis taking into account delayed rediploidization that its octoploid genome composition results from two rounds of homologous whole genome duplications (WGDs), and further provide insight into the timing of its ploidy evolution. This study provides the first octoploid genome resource of Acipenseriformes for understanding ploidy composition and evolutionary trajectories of polyploidy fishes.