Endogenous viral elements trace the ancient origins and early evolution of the Caulimoviridae.

Endogenous viral elements (EVEs) are viral sequences integrated into host genomes, functioning as molecular fossils of past infections. Most characterised EVEs in plants are derived from the Caulimoviridae, the only family of dsDNA viruses infecting this kingdom. Endogenous caulimovirids (ECVs) occur across taxonomically diverse vascular plant species and represent a significant resource for studying host-virus coevolution, host range dynamics, and the evolution of viral genomes over deep timescales. Previous evolutionary studies utilising ECVs have proposed cospeciation or host switching as the primary drivers of Caulimoviridae diversification; however, these studies were limited by poor representation of genomic data from basal plant lineages. Here, we analysed 93 plant genomes spanning all major embryophyte groups, including ferns and lycophytes, and identified 47,135 ECVs across 75 genomes. These sequences were classified into 71 operational taxonomic units (OTUs), including 35 previously undescribed groups, revealing substantial and previously unrecognised diversity within the Caulimoviridae. Notably, we identified a basal clade restricted to the Araucariaceae, an ancient lineage of Gondwanan conifers. Phylogenetic comparisons between ECVs and host plant lineages support a macroevolutionary model in which cospeciation with tracheophytes played a dominant role in shaping Caulimoviridae diversification. Together, these findings establish Caulimoviridae and their endogenous counterparts as a powerful model system for paleovirology, offering unprecedented insights into the coevolution, diversification, and extinction of plant viruses over deep evolutionary timescales.