Host hybridization enabled the emergence of a reassorted hantavirus lineage

The exchange of genetic material between individuals is a key driver of evolution and diversification across most branches of life. Segmented viruses can exchange genetic material through reassortment of genomic segments. New viral strains that emerge from reassortments can have greater infection ranges and higher virulence, although concrete examples of the adaptive advantages of reassortants in nature apart from influenza remain rare. We studied here the evolutionary history and consequences of reassortment in Tula orthohantavirus (TULV) in a hybrid zone between evolutionary lineages of its reservoir host, the common vole ( Microtus arvalis ). Across 58 trapping sites and 127 infected voles, we detected 27 TULV reassortants in a 12.5 km broad zone at the contact of the parental TULV clades, resembling a viral hybrid zone concordant with the hosts’. Phylogenomic analyses revealed three independent reassortment events, but most of the host hybrid zone was dominated by a single strain with a reassorted M-Segment, which encodes the surface glycoprotein. We detected clade-specific variation in the glycoprotein’s N-terminal region consisting of five residues, two of which showed evidence of positive selection. In silico 3D modeling of seven glycoproteins confirmed that this N-terminal region has a unique and specific structure for each TULV clade and the dominant reassortants and is the only structurally variable region of the TULV glycoprotein. Our findings suggest that reassortment between the parental TULV clades in the contact region has resulted in a transgressive virus phenotype potentially adapted to hybrid hosts. This demonstrates the potential of zones of hybridization for the emergence of new virus strains with novel evolutionary trajectories.