Historical and contemporary factors driving the evolution of host specialisation in disease vectors – ESPEVEC

We sample the tick species from across their geographic range on different host species. Precise measurements are taken to quantify tick body size and shape and analyses are performed to characterize the chemical signals used by ticks to attract mates. Finally, all ticks are characterized genetically. With these data, we test whether differences among ticks can be directly attributed to host use. We then test whether the divergence among tick populations using different host species changes the risk of transmitting specific pathogens.

We have found that ticks very frequently specialize on different host species within the local environment, even if they do not always evolve into different species. This means that certain ticks feed preferentially on certain hosts, creating a barrier to pathogen transmission and altering predicted transmission pathways. Our results at a large spatial scale also suggest that this specialization is partly due to selection pressure from the host that changes tick body size and form. We have also discovered that in addition to pathogens, ticks harbor a wide array of bacterial endosymbionts. We don’t yet know the ecological effects of these bacteria on host use in ticks, but we have demonstrated that these organisms may emerge into vertebrate pathogens. This is particularly the case for Coxiella bacteria that are responsible for Q fever; the pathogen Coxiella burnetii has evolved directly from related bacteria found in seabird ticks.

Although focused on tick systems, we expect that the results of this project will alter the general view of vector-borne disease ecology. As the evolution of distinct vector groups can create several semi-independent transmission cycles at a local scale, and given that these cycles may represent different transmission risks to humans, the results of our work will determine the degree to which local host use will need to be taken into explicit consideration for making predictions about disease epidemiology. Likewise, the identification of ecological factors favouring vector specialisation should provide important elements for our understanding of vector-borne disease epidemiology. Finally, given current uncertainty about the impact of climate change and landscape modifications on infectious disease emergence, the fundamental and applied results of this project will provide essential contributions to integrative networks that aim to use environmental and epidemiological data to establish proactive public health responses to potential disease threats.

Several presentations (15) and major scientific publications (7) have already been produced in the context of this project. In particular, using genetic data, we have retraced the world-wide colonization route of the seabird tick Ixodes uriae from its initial divergence in the southern hemisphere. This analysis has demonstrated that ticks diversified in direct response to the diversification of seabirds and that the tick host races found within each ocean basin have evolved independently (Dietrich et al. 2014 Molecular Ecology). We have shown in both soft tick and hard tick systems that host specialization readily occurs, but does not always result in the evolution of novel species (Dupraz et al. 2016 Infect. Genet. Evol). We have also shown (Duron et al. 2015 PlosPathogens) that the infectious agent responsible for Q fever (Coxiella burnetii) emerged from a tick endosymbiont (an intracellular bacterium that normally does not come into contact with the vertebrate that ticks feed on). This provides a novel framework for understanding pathogen emergence.

Vector-borne diseases are often maintained in complex transmission cycles that include several vectors and different reservoir host species. However, to date, we know little about how vectors adapt to different local host species and how this may in turn affect pathogen dynamics and disease risk. In the case of systems where numerous host species are available, it is therefore essential to establish whether vectors specialise to exploit different hosts and the role of these different local host-vector systems in pathogen transmission and evolution. It is also critical to identify the ecological factors and evolutionary mechanisms that lead to vector specialisation if we are to better predict pathogen transmission in a changing landscape. The ESPEVEC project aims to tackle these questions using three contrasting host-vector-pathogen systems involved in tick-borne disease and a highly qualified international research consortium consisting of 4 partner laboratories and several international collaborating institutes.

The three tick systems to be studied are all of particular medical and economic interest, involving two hard tick vectors of Lyme borreliosis (Ixodes ricinus and Ixodes uriae) and one soft tick vector of human relapsing fever (Ornithodoros capensis complex). These systems vary in both their ecological characteristics and evolutionary histories enabling us to evaluate the relative contribution of different factors to overall patterns of host-associated vector divergence.

Within the framework of the project, we will test the general hypothesis that the evolution of host-associated structure in ticks varies with the composition and history of the local host-vector community. The first two project tasks will evaluate within-community genetic structure of ticks across replicate sites in relation to host use, retrace these patterns using a phylogeographic framework and contrast results for different tick systems. We predict that host-associated structure should increase with the evolutionary age and stability of the local host community. Next, we will examine the mechanisms behind patterns of local divergence via genotypic and phenotypic patterns of variation. More specifically, morphometrical and chemical analyses will be performed to identify the potential selective forces responsible for host-associated divergences and will be completed by a genome-wide screening of divergence among host-associated groups. Finally, we will investigate the consequences of this structure for pathogen circulation and evolution at different spatial scales by typing selected bacterial pathogens within the sampled communities and comparing patterns of infection and population structure in the pathogen with that in the vector and hosts. This work will rely on a combination of field sampling, experimental quantifications, and modern approaches for quantifying phenotypic and genetic characteristics.

Although applied to tick systems, we expect that the results of this project will alter the general view of vector-borne disease ecology. By combining results from the different project tasks, we will be able to 1) better understand vector-borne disease ecology and the origins of vector and pathogen diversity, 2) evaluate the relative role of different component species in disease risk and thus determine the importance of incorporating local divergence patterns into epidemiological models of disease risk, and 3) obtain essential information on how landscape modifications and species redistributions may alter pathogen emergence.