Swali, P.; Booth, T.; Tan, C. C. S.; McCabe, J.; Anastasiadou, K.; Barrington, C.; Borrini, M.; Bricking, A.; Buckberry, J.; Buster, L.; Carlin, R.; Gilardet, A.; Glocke, I.; Irish, J.; Kelly, M.; King, M.; Petchey, F.; Peto, J.; Silva, M.; Speidel, L.; Tait, F.; Teoaca, A.; Valoriani, S.; Williams, M.; Madgwick, R.; Mullan, G.; Wilson, L.; Cootes, K.; Armit, I.; Gutierrez, M. G.; van Dorp, L.; Skoglund, P.

Several disease-causing bacteria have transitioned from tick-borne to louse-borne transmission, a process associated with increased virulence and genome reduction. However, the historical time frame and speed of such evolutionary transitions have not been documented with ancient genomes. Here, we discover four ancient cases of Borrelia recurrentis, the causative agent of louse-borne relapsing fever, in Britain between ~600 and 2,300 years ago, and sequence whole genomes up to 29-fold coverage. We estimate a recent divergence from the closest tick-borne ancestor, likely within the last ~8,000 years. We reconstruct a chronology of gene losses and acquisitions using the pan-genome of related species, and show that almost all of the reductive evolution observed in B. recurrentis had occurred by ~2,000 years ago, and was thus a rapid process after divergence. Our observations provide a new understanding of the origins of B. recurrentis and document complex reductive evolution in a specialist vector-borne pathogen.