Abstract
Obligatory hematophagous arthropods such as lice, bugs, flies, and ticks harbor bacterial endosymbionts that are expected to complement missing essential nutrients in their diet. Genomic and some experimental evidence support this expectation. Hard ticks (Acari: Ixodidae) are associated with several lineages of bacterial symbionts, and very few were experimentally shown to be essential to some aspects of tick’s fitness. In order to pinpoint the nature of interactions between hard ticks and their symbionts, we tested the effect of massive elimination of Coxiella-like endosymbionts (CLE) by antibiotics on the development and fitness of the brown dog tick (Rhipicephalus sanguineus). Administration of ofloxacin to engorged (blood fed) nymphs resulted in significant and acute reduction of their CLE loads – an effect that also persisted in subsequent life stages (aposymbiotic ticks). As a result, the post-feeding development of aposymbiotic female (but not male) nymphs was delayed. Additionally, aposymbiotic adult females needed a significantly prolonged feeding period in order to replete (detach from host), and had reduced engorgement weight and a lower capacity to produce eggs. Consequently, their fecundity and fertility were significantly reduced. Eggs produced by aposymbiotic females were free of CLE, and the resulting aposymbiotic larvae were unable to feed successfully. Our findings demonstrate that the observed fitness effects are due to CLE reduction and not due to antibiotic administration. Additionally, we suggest that the contribution of CLE is not mandatory for oocyte development and embryogenesis, but is required during feeding in females, when blood meal processing and tissue buildup are taking place. Presumably, under these extreme physiological demands, CLE contribute to R. sanguineus through supplementing essential micro- and macronutrients. Further nutrient complementary studies are required to support this hypothesis.
Highlights
Arthropods that feed exclusively on restricted diets such as plant sap or vertebrate blood rely on microbial symbionts to supplement missing essential nutrients in their diet (Buchner, 1965)
Few studies examined the fitness consequences associated with elimination of endosymbionts in hard ticks (Zhong et al., 2007; Guizzo et al., 2017; Zhang et al., 2017; Li et al., 2018)
A similar trend of the essential contribution of Coxiella-like endosymbionts (CLE) to the well-being of its host is consistent across those studies, it is difficult to compare them to our study
Summary
Arthropods that feed exclusively on restricted diets such as plant sap or vertebrate blood rely on microbial symbionts to supplement missing essential nutrients in their diet (Buchner, 1965) Such nutritional symbioses are ubiquitous in obligatory blood feeders like Tsetse flies and bedbugs, where bacterial symbionts synthesize B vitamins lacking in the blood meal All CLE genomes studied so far are reduced in size and retain some functional pathways for synthesizing B vitamins (Gottlieb et al, 2015; Smith et al, 2015; Guizzo et al, 2017; Tsementzi et al, 2018) This is the case in studied genomes of tickassociated Francisella-like endosymbionts (Gerhart et al, 2016; Duron et al, 2018)
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