Population Genetic Analysis Reveals Recent Demographic Expansion and Local Differentiation of Areca Palm Velarivirus 1 in Hainan Island

Areca palm velarivirus 1 (APV1), the causal agent of yellow leaf disease (YLD), poses a serious threat to the economically important areca palm industry in the Hainan Province, China, yet its evolutionary dynamics remain poorly understood. Here, we performed a large-scale molecular survey by sequencing the coat protein (CP) gene from 364 APV1-infected samples collected across major cultivation regions of Hainan. Population genetic analyses revealed extremely high haplotype diversity (Hd = 0.997) but very low nucleotide diversity (π = 0.017). Neutrality tests (Tajima’s D = −2.266; Fu’s FS = −23.697) and a unimodal mismatch distribution supported a scenario of recent demographic expansion from a restricted ancestral pool. Evolutionary analyses indicated that the CP gene is subject to strong purifying selection, although eight codons exhibited episodic positive selection, suggesting ongoing viral adaptation. Furthermore, we identified three distinct genetic clusters with significant geographic structuring, indicating that viral dissemination is shaped by local factors. Together, these results reveal a recent explosive invasion of APV1 characterized by rapid island-wide expansion and emerging local differentiation. This work provides novel insights into the evolutionary trajectory of APV1 and establishes a genomic basis for improved surveillance and management of YLD.