Tick-pathogen Ensembles: Do molecular interactions lead ecological innovation?

Ticks are arthropods distributed worldwide that constitute the most important vectors of diseases to animals, and second to mosquitoes regarding pathogens of public health importance. Ticks are remarkably plastic and can colonize diverse ecological niches of the planet, from tropics to polar areas (de la Fuente et al., 2008). In the last decade, the reports of tick-borne pathogens have increased sharply, motivating vigorous research programs that addressed major questions on the epidemiology of tick-borne diseases, vector-host-pathogen interactions, tick ecology, and tick genomics. Notably, the first tick genome was released this year (Gulia-Nuss et al., 2016), opening new possibilities to explore tick-host-pathogen interactions (de la Fuente et al., 2016a). In contrast, the evolutionary and ecological implications of tick-pathogen associations have received comparatively less attention. Herein, we hypothesized that tick-pathogen associations evolved to form “intimate epigenetic relationships” similar to those described for Theileria spp. and its vertebrate host (Cheeseman and Weitzman, 2015) in which the pathogen induces transcriptional reprogramming in infected ticks. This will ultimately favor pathogen propagation, but will also select for the most suitable ecological adaptations in the tick vector. These phenotypic and genetic changes may have the potential to be transmitted to the next generation of ticks. As a result, the ecological associations between tick, vertebrates, and pathogens would evolve to maximize pathogen circulation in these communities (Estrada-Peña et al., 2015, 2016). Our hypothesis was based on the following evidences: (i) tick-borne pathogens induce transcriptional reprogramming in infected tick (Ayllón et al., 2015; Villar et al., 2015; Weisheit et al., 2015) and vertebrate cells (Lee et al., 2008; Bouquet et al., 2016); (ii) tick-borne pathogens produce and secrete effector proteins, nucleomodulins, which constitute a family of proteins produced by bacterial pathogens to control host transcription and other nuclear processes (Bierne and Cossart, 2012), that interact with host epigenetic machinery and induce transcriptional reprogramming (Garcia-Garcia et al., 2009a, b; Rennoll-Bankert et al., 2015; Sinclair et al., 2015; Lina et al., 2016), and (iii) tick-pathogen interactions increase tick fitness (Neelakanta et al., 2010; Belova et al., 2012; Herrmann and Gern, 2015; de la Fuente et al., 2016b)