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Co-evolution and implications of vector adaptation: A case study on seabird ticks and Borrelia

Final Report Summary - COSEATIBO (Co-evolution and implications of vector adaptation: a case study on seabird ticks and Borrelia)

The emergence of infectious diseases is often attributed to the adaptation of parasitic organisms to new hosts. In the case of vector-borne disease, pathogen transmission, and thus access to novel host types, will be strongly constrained by host use of the vector. In this way, host-associated specialisations in the vector organism can be a major factor mediating the evolution of the pathogens they transmit. The principal goal of this project was to investigate mechanisms of host specialisation in vectors and understand how it affects pathogen transmission, disease epidemiology and, ultimately, parasite evolution.

To do this, we considered two parallel seabird-tick systems, Ixodes uriae and the species complex Ornithodoros capensis. Both ticks use a diverse range of colonial seabird species as hosts and both can transmit bacteria of the genus Borrelia. As these bacteria are responsible for diseases such as Lyme disease and Relapsing fever in humans, an understanding of their epidemiology, and in particular the role of seabirds in their large scale spread, is essential.

Following the discovery of repeated patterns of host-associated divergence in the polar seabird tick, Ixodes uriae, we first investigated the phylogeography of the tropical seabird tick complex Ornithodoros capensis. More than 150 O. capensis ticks from around the globe were typed and analysed at one mitochondrial (16S rRNA) and one nuclear gene (18S rRNA).

We found a much higher genetic diversity than expected according to previous morphological identifications and several cryptic species could be identified within a single geographic location (i.e. presence of cryptic species in sympatry). At a large spatial scale, geographic distance clearly plays an important role in determining the spatial structure of these ticks. At a more local scale, tick populations structured by host species, suggesting that host specialisation has also likely played a major role in the diversification of the complex.

In order to fully consider the consequences of population structure and host use for disease epidemiology, we carried out a literature review of what is known about seabird ticks, their dispersal patterns and the pathogens they carry (Dietrich et al., 2010). Clearly, seabird tick systems may harbour an important diversity of pathogens that can interact with terrestrial systems.

In the next part of the project, we aimed to characterise patterns of prevalence and infection intensity of Borrelia bacteria among different host races in several geographic locations. By combining novel statistical methods (i.e. site-occupancy modelling) and a quantitative PCR approach, we showed the existence of strong biases in the probability of detecting Lyme disease bacteria in the different tick host races. These biases can lead to a significant underestimation of Borrelia prevalence in the vector ticks and are due to differences in the intensity of infection of Borrelia bacteria among I. uriae host races.

From this data, it is clear that certain seabird species - tick race combinations are more important than others for the large-scale circulation of the pathogen. This work also suggests that similar patterns may be present in other vector-borne disease systems and that host specialisation in the vector requires more explicit consideration in these systems. This study has been recently published in Evolutionary Applications (Gomez-Diaz et al., 2010).

Finally, we investigated patterns of genetic diversity and population structure of marine Borrelia bacteria in different seabird-host races and multiple geographic locations with the aim of understanding the diversity, evolution and interaction with terrestrial disease systems. Initial studies indicated the presence of several Borrelia species in marine polar systems, but that most seabird colonies were dominated by the species Borrelia garinii (Duneau et al., 2008, Dietrich et al., 2008).

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