Demographic expansions and the emergence of host specialization in genetically distinct strains of the tick-transmitted bacteriumAnaplasma phagocytophilum

ABSTRACT Bacteria species that must obligately replicate in vertebrate host cells make up a large proportion of the prokaryotic pathogens with human and veterinary health implications. In such bacterial taxa, extrinsic processes play an important role in influencing the phylogenetic diversity of viable hosts (‘host range’). These processes include both changes in host population densities and shifts in host geographic distributions. In Europe, distinct genetic strains of the tick-vectored bacterium Anaplasma phagocytophilum circulate among mammals in three discrete enzootic cycles. To date, the factors that contributed to the emergence of these strains have been poorly studied. Here we show that the strain which predominately infects roe deer ( Capreolus capreolus ) is evolutionarily derived. Its divergence from a likely host-generalist ancestor occurred after the last glacial maximum as mammal populations, including roe deer, recolonized the European mainland from southern refugia. We also provide evidence that this host-specialist strain’s effective population size (N e ) has tracked changes in the population of its roe deer host. Specifically, both host and bacterium appear to have undergone substantial increases in N e over the past 1,500 years. In contrast, we show that while it appears to have undergone a major population expansion starting ∼3,500 years ago, in the past 500 years the contemporary host-generalist strain has experienced a substantial reduction in genetic diversity levels, possible as the result of reduced transmission opportunities between competent hosts. IMPORTANCE The findings of this study are some of the first to examine specific events in the evolution of host specialization in a naturally occurring, obligately intracellular bacterial species. They show that host range shifts and the emergence of host specialization may occur during periods of population growth in a host-generalist ancestor. The results discussed here also show the close correlation between demographic patterns in host and pathogen for a specialist system. These findings have important relevance for our understanding of the evolution of host-range diversity. They may inform future work on host-range dynamics and provide insights for understanding the emergence of pathogens which have human and veterinary health implications.