Phylogeographic relationships and the evolutionary history of the Carassius auratus complex with a newly born homodiploid raw fish (2nNCRC)

BACKGROUND: An important aspect of studying evolution is to understand how new species are formed and their uniqueness is maintained. Hybridization can lead to the formation of new species through reorganization of the adaptive system and significant changes in phenotype. Interestingly, eight stable strains of 2nNCRC derived from interspecies hybridization have been established in our laboratory. To examine the phylogeographical pattern of the widely distributed genus Carassius across Eurasia and investigate the possible homoploid hybrid origin of the Carassius auratus complex lineage in light of past climatic events, the mitochondrial genome (mtDNA) and one nuclear DNA were used to reconstruct the phylogenetic relationship between the C. auratus complex and 2nNCRC and to assess how demographic history, dispersal and barriers to gene flow have led to the current distribution of the C. auratus complex. RESULTS: As expected, 2nNCRC had a very close relationship with the C. auratus complex and similar morphological characteristics to those of the C. auratus complex, which is genetically distinct from the other three species of Carassius. The estimation of divergence time and ancestral state demonstrated that the C. auratus complex possibly originated from the Yangtze River basin in China. There were seven sublineages of the C. auratus complex across Eurasia and at least four mtDNA lineages endemic to particular geographical regions in China. The primary colonization route from China to Mongolia and the Far East (Russia) occurred during the Late Pliocene, and the diversification of other sublineages of the C. auratus complex specifically coincided with the interglacial stage during the Early and Mid-Pleistocene in China. CONCLUSION: Our results support the origin of the C. auratus complex in China, and its wide distribution across Eurasia was mainly due to natural Pleistocene dispersal and recent anthropogenic translocation. The sympatric distribution of the ancestral area for both parents of 2nNCRC and the C. auratus complex, as well as the significant changes in the structure of pharyngeal teeth and morphological characteristics between 2nNCRC and its parents, imply that homoploid hybrid speciation (HHS) for C. auratus could likely have occurred in nature. The diversification pattern indicated an independent evolutionary history of the C. auratus complex, which was not separated from the most recent common ancestor of C. carassius or C. cuvieri. Considering that the paleoclimate oscillation and the development of an eastward-flowing drainage system during the Pliocene and Pleistocene in China provided an opportunity for hybridization between divergent lineages, the formation of 2nNCRC in our laboratory could be a good candidate for explaining the HHS of C. auratus in nature. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08468-x.