Genome duplication and regulatory innovation underpin contrasting life-history strategies in cryptic Cassytha filiformis lineages.

BACKGROUND AND AIMS: Parasitic plants have evolved extreme adaptations, but the origins of these innovations remain poorly understood. Cassytha filiformis is a leafless stem hemiparasite representing an ancient angiosperm lineage with pantropical distribution. Plastome studies revealed cryptic lineages in South China and Southeast Asia, but the nuclear genomic basis remains unclear. METHODS: We combined comparative transcriptomics, phylogenomics, and common-garden phenotypic assays to investigate genome dynamics and cryptic divergence. We quantified transcriptomic divergence via orthologous gene family comparisons, detected gene duplications using Ks distributions, and assessed functional enrichment of parasitism-related duplicates; germination and parasitic vigor were measured under greenhouse conditions. KEY RESULTS: Nuclear phylogenomic analyses showed that morphologically indistinguishable lineages diverged in the Late Miocene, significantly later than plastid-based estimates, indicating decoupled organellar and nuclear evolutionary rates. The lineages exhibited highly asymmetric transcriptomic divergence, with less than 30% of gene families forming a conserved core transcriptome. We identified recent, lineage-specific gene duplications (Ks=0.2-0.4) that provided raw material for parasitism, with 67% and 76% of known parasitism-related genes in each lineage arising from these duplicates. Functional enrichment highlighted convergence in hormone signaling and regulatory pathways. CONCLUSIONS: This genomic divergence mirrors distinct life-history strategies, one lineage invests more in propagule establishment (higher germination), while the other prioritizes rapid host exploitation (greater parasitic vigor). Our study demonstrates that regulatory innovation and gene duplication underpin ecological divergence and parasitic adaptation in this ancient hemiparasitic lineage.