Recurrent evolution of host and vector association in bacteria of the Borrelia burgdorferi sensu lato species complex

Abstract

Background: The Borrelia burgdorferi sensu lato (s.l.) species complex consists of tick-transmitted bacteria and currently comprises approximately 20 named and proposed genospecies some of which are known to cause Lyme Borreliosis. Species have been defined via genetic distances and ecological niches they occupy. Understanding the evolutionary relationship of species of the complex is fundamental to explaining patterns of speciation. This in turn forms a crucial basis to frame testable hypotheses concerning the underlying processes including host and vector adaptations.

Results: Illumina Technology was used to obtain genome-wide sequence data for 93 strains of 14 named genospecies of the B. burgdorferi species complex and genomic data already published for 18 additional strain (including one new species) was added. Phylogenetic reconstruction based on 114 orthologous single copy genes shows that the genospecies represent clearly distinguishable taxa with recent and still ongoing speciation events apparent in Europe and Asia. The position of Borrelia species in the phylogeny is consistent with host associations constituting a major driver for speciation. Interestingly, the data also demonstrate that vector associations are an additional driver for diversification in this tick-borne species complex. This is particularly obvious in B. bavariensis, a rodent adapted species that has diverged from the bird-associated B. garinii most likely in Asia. It now consists of two populations one of which most probably invaded Europe following adaptation to a new vector (Ixodes ricinus) and currently expands its distribution range.

Conclusions: The results imply that genotypes/species with novel properties regarding host or vector associations have evolved recurrently during the history of the species complex and may emerge at any time. We suggest that the finding of vector associations as a driver for diversification may be a general pattern for tick-borne pathogens. The core genome analysis presented here provides an important source for investigations of the underlying mechanisms of speciation in tick-borne pathogens.

Keywords: Borrelia burgdorferi sensu lato; Evolution; Host association; Lyme disease; Population genomics; Vector adaptation.

Fig. 1

Phylogenetic inference and main host and vector association of B. burgdorferi sensu lato The phylogeny reconstructed with BEAST v1.7.5 [26] is based on 114 orthologous single copy genes. Genospecies names and host associations are indicated next to the cluster. As huge number of host species can serve as reservoirs for Borrelia [4], for sake of clarity, we used a crude host association referring to rodents (indicated by the mouse), birds (indicated by the black bird) and lizards. For the same reason, not all vector associations can be shown. The following vectors are not shown in the phylogeny (which does not mean that they are less important for natural transmission cycles): I. hexagonus (vector of B. afzelii, B. burgdorferi s.s., B. bavariensis), I. affinis (B. burgdorferi s.s., B. bissettiae), I. minor (B. americana, B. carolinensis), I. jellisoni (B. californiensis), I. uriae, I. pavlovskyi (B. garinii), I. stilesi (B. chilensis) and I. granulatus (B. yangtzensis) and I. nipponensis. Note the high posterior probability of internal nodes (within-species node posterior probabilities are not shown for sake of clarity). The scale bar indicates substitutions per site