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Despite the importance of population structure for the epidemiology of pathogenic bacteria, the spatial and ecological heterogeneity of these populations is often poorly characterized. Here, we investigated the genetic diversity and population structure of the Lyme borreliosis (LB) spirochaeteBorrelia gariniiin its marine cycle involving colonial seabirds and different host races of the seabird tickIxodes uriae. Multilocus sequence analyses (MLSA) on eight chromosomal and two plasmid loci (ospAandospC) indicate thatB. gariniicirculating in the marine system is highly diverse. Microevolution in marineB. gariniiseems to be mainly clonal, but recombination and selection do occur. Sequence types were not evenly distributed among geographic regions, with substantial population subdivision between Atlantic and Pacific Ocean basins. However, no geographic structuring was evident within regions. Results of selection analyses and phylogenetic discordance between chromosomal and plasmid loci indicate adaptive evolution is likely occurring in this system, but no pattern of host or vector-associated divergence was found. Recombination analyses showed evidence for population admixture between terrestrial and marine strains, suggesting that LB spirochaetes are exchanged between these enzootic cycles. Importantly, our results highlight the need to explicitly consider the marine system for a complete understanding of the evolutionary ecology and global epidemiology of Lyme borreliosis.