The diversity and host range of endogenous caulimovirids illuminate the ancient origin and early evolution of the Caulimoviridae

Endogenous viral elements (EVEs) are viral sequences integrated into the genomes of host organisms, analogous to molecular fossils. The majority of 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 based on ECVs proposed either cospeciation or host-switching as the main drivers of Caulimoviridae evolution, but were limited by sparse genomic data from basal plant lineages. Using 93 plant genomes spanning all embryophyte lineages, including ferns and lycophytes, we identified 47,135 ECVs in 75 genomes. These were grouped into 71 operational taxonomic units (OTUs), including 35 novel ones, revealing unexpected Caulimoviridae diversity in vascular plants and a new clade restricted to gymnosperms. Phylogenetic comparisons with host plant taxonomy support a macroevolutionary scenario in which cospeciation with tracheophytes drove the diversification of Caulimoviridae. Our findings position Caulimoviridae and ECVs as a reference system for paleovirology, offering unprecedented insights into how plant viruses and their hosts coevolved, diversified, and sometimes went extinct.