Osteoglossid pangenome reveals ancient teleost evolution and population dynamics

Osteoglossidae, one of the most ancient freshwater fishes exhibiting transcontinental disjunction, offers important insights into early teleost evolution and historical biogeography. Utilizing integrated sequencing strategies, we reported two T2T chromosome-level genome assemblies for pirarucu (Arapaima gigas) and Australian bonytongue (Scleropages jardinii) and a near T2T genome assembly for black arowana (Osteoglossum ferreirai). The BUSCO completeness was >97% for all the assemblies, markedly surpassing most of the previous osteoglossid assemblies. Using these reference genomes, we reconstructed a time-calibrated phylogeny, defined the major divergence time and evaluated the vicariance hypotheses related to Gondwana. We found that the divergence between Osteoglossum and Scleropages is estimated at 52.6 Mya, supporting that their vicariant events may have resulted from the separation of Australia from the Antarctica–South America landmass. In addition, we reconstructed the ancestral karyotypes of Scleropages and Osteoglossum, revealing five and ten major chromosomal rearrangements, respectively. We further systematically reconstructed and parsed the historical population dynamics across most of the Osteoglossidae species, demonstrating dramatic declines in effective population sizes for most Osteoglossidae species during the Last Glacial Period. Together, our findings offer a comprehensive genomic perspective into the evolutionary history, genome architecture, and historical biogeography of Osteoglossidae while also providing essential resources for future conservation and research.