Population Genomics of Megalobrama Provides Insights into Evolutionary History and Dietary Adaptation

SIMPLE SUMMARY: Megalobrama is the economically most important freshwater fish genus in China. In recent years, germplasm resources of Megalobrama have been depleting as a result of environmental degradation and artificial factors. In this study, we established the whole genome database of Megalobrama populations using the whole genome re-sequencing technology, explored population genetic structure, and inferred comprehensive evolutionary relationships using principal component analysis and population structure analysis. Furthermore, employing selective sweep analysis, we identified candidate genes related to variations in feeding habits, revealing the molecular mechanisms of environmental adaptability in Megalobrama populations. Taken together, this study describes the population history and genetic diversity of Megalobrama populations and also the molecular mechanisms likely involved their environmental adaptability. These findings will make a substantial contribution to conservation and utilization of Megalobrama germplasm resources. ABSTRACT: Megalobrama, a genus of cyprinid fish, is an economically important freshwater fish widely distributed in major waters of China. Here, we report the genome resequencing of 180 Megalobrama fish including M. amblycephala, M. skolkovii, M. hoffmanni, and M. pellegrini. Population structure indicated that geographically divergent Megalobrama populations were separated into six subgroups. A phylogenetic tree showed that M. skolkovii was more closely related to M. pellegrini than other species and M. hoffmanni was clustered apart from other Megalobrama species, showing a high nucleotide diversity in geographic groups. Treemix validated gene flow from M. amblycephala to M. skolkovii, suggesting that introgression may provide an important source of genetic variation in the M. skolkovii populations. According to the demographic history analysis, it is speculated that Megalobrama might have been originally distributed in the Pearl River with some spread to Hainan Island and northern China due to lower sea levels during the glacial period. Whole-genome selective sweeps analysis demonstrated that M. amblycephala likely developed an enhanced energy metabolism mostly through fatty acid degradation pathways whereas M. hoffmanni possibly regulate lipid absorption via the cholesterol metabolism pathway. Taken together, this study provides a valuable genomic resource for future genetic investigations aiming to improve genome-assisted breeding of Megalobrama species.