Unravelling the genetic landscape of Channa argus in Shandong Province: Insights into population differentiation, adaptation and conservation from whole-genome resequencing.

Abstract

The snakehead (Channa argus) is an economically important freshwater fish species. Understanding how geographical isolation affects population differentiation is important for understanding the processes that shape biodiversity. We examined four wild populations [Dongping Lake (DP), Nansi Lake (NS), Yihe River (YH) and Yellow River Estuary (HH)] and an aquaculture population [Weishan Lake (WL)] in Shandong Province using whole-genome resequencing for the first time. This approach provided deeper insights of genetic variation compared to previous studies with lower genome coverage. We identified single nucleotide polymorphisms (SNPs) and insertion-deletion (InDel) variants among the five populations. A total of 106,172 DNA variants were located in the exonic gene region, with 53,415 causing nonsynonymous mutations, 9757 resulting in frameshift mutations and 2345 leading to a loss or gain of stop codons. Polymorphic information content (PIC) analysis showed moderate polymorphism across all populations, with an increase over the past decade, likely due to reduced human interference. Genetic diversity indexes (H_O, H_E, H' and π) showed minimal variation among populations, suggesting similar environmental pressures and low levels of inbreeding. F_is values indicated that the WL and NS populations met the neutral expectation of heterozygosity, whereas other populations exhibited higher heterozygosity potentially due to geographical factors. Phylogenetic tree analysis, principal component analysis (PCA) and population structure analysis confirmed genetic clustering aligned with geographical distribution. The F_st values indicated moderate genetic differentiation, with gene flow observed between the DP and WL populations likely due to artificial introductions. The WL population exhibited strong signs of artificial selection. Functional enrichment analysis revealed adaptive differentiation in osmoregulation-related genes in the HH population, whereas the WL population showed selective pressure in genes related to oxygen transport in the blood, suggesting the influence of aquaculture and environment on genetic adaptation. This study highlights the role of geographical isolation in population differentiation and emphasizes the importance of habitat connectivity in maintaining gene flow and genetic diversity. The findings indicate no significant human-induced isolation in the major water bodies of Shandong Province, which benefits the conservation of C. argus and provides valuable insights for the sustainable management of wild populations.