Population Genomics Provides Novel Insights Into Evolutionary Relationships and Local Adaptation of Two Ecotypes...

Coilia nasus is an economically important fish species that exhibits two distinct life history strategies: an anadromous form, which migrates from seawater to freshwater to spawn, and a freshwater-resident form that completes its entire life cycle in freshwater habitats. The taxonomic status of the freshwater-resident form (C. nasus taihuensis) has long remained unresolved, as it is unclear whether it represents a distinct subspecies or a divergent ecotype. To explore the evolutionary relationships between anadromous and freshwater-resident forms, we performed whole-genome resequencing of 12 geographical populations from the Yangtze River, Huaihe River, and Yellow River systems and obtained 8,701,537 high-quality single nucleotide polymorphisms (SNPs). Based on multiple analyses (NJ tree, PCA, and ADMIXTURE analysis), our study confirmed that C. nasus taihuensis is not a valid subspecies but rather a freshwater ecotype of C. nasus. Compared to anadromous C. nasus, freshwater-resident C. nasus taihuensis exhibited slightly higher genetic diversity, an elevated Tajima's D value, and lower levels of linkage disequilibrium, suggesting potential differences in demographic history and selective pressures. The estimated divergence time of approximately 4.6 thousand years ago between the two ecotypes coincides with the geological formation of Tai Lake. Whole-genome scans identified 290 selective sweep genes that underlie local adaptation in anadromous C. nasus. Several candidate genes were mainly involved in energy metabolism (SCD, HOAD, and DEGS2) and osmoregulation (CLCN4, IGF2, and LRP1), suggesting their potential contribution to highly efficient long-distance migration and adaptation to seawater. In contrast, freshwater-resident C. nasus taihuensis exhibited strong signatures of selection in genes related to osmotic and ionic balance (ATP1A1, AQP9, NBC, NHE3, and CA4), which may have driven the genetic divergence of this ecotype. Our comprehensive study provides valuable insights into the genetic basis of C. nasus, with critical implications for further conservation efforts of this ecologically valuable fish.