Whole-genome resequencing reveals genetic divergence, local adaptation, and conservation priorities in three helmet catfishes (complex Cranoglanis bouderius)

This study employed whole-genome resequencing to investigate the genetic diversity, population structure, and adaptive evolution of three geographically isolated populations of helmet catfish (Cranoglanis bouderius). These populations are distributed across the Pearl River Basin (CB) in mainland China, Hainan Island (CM), and the Red River Basin in Vietnam (CH). Despite minimal observable morphological divergence, our analysis revealed significant genetic differentiation among the populations. The CM and CH populations exhibited closer genetic affinity, likely resulting from historical biogeographic connections through the Red River Fault Zone. In contrast, the CB population was genetically more distinct. Genome-wide single nucleotide polymorphism (SNP) analysis indicated that the CB population possesses the lowest genetic diversity, while the CH population possesses the highest. This pattern is inconsistent with previous findings based on mitochondrial DNA (mtDNA). Demographic history reconstruction using the Pairwise Sequentially Markovian Coalescent (PSMC) model suggested that all three populations experienced declines during the Pleistocene glaciations. However, the CB population exhibited a more pronounced post-glacial recovery, potentially due to its inland distribution. Estimates of recent effective population size (Nₑ) from the software GONE, spanning 50 to 750 generations, revealed a contrasting trend. The CH population currently maintains a larger Nₑ than the CB population. This combination of a smaller recent Nₑ and reduced genetic diversity in the CB population underscores the urgent need for targeted conservation strategies to ensure its long-term persistence. Functional enrichment analysis (KEGG) further identified distinct adaptive signatures among the populations. Adaptive evolution in viral and immune-related pathways was detected in the CB and CH populations, likely shaped by elevated pathogen pressure in their habitats. Conversely, the CM population showed adaptive enrichment in pathways associated with metabolism and nervous system development. This finding is consistent with its more isolated and resource-constrained environment. These results highlight the profound role of long-term geographic isolation and environmental selection in driving genetic and functional divergence. They also provide critical insights for the informed conservation and management of C. bouderius populations.