Ticks are obligatorily hematophagous but spend the majority of their lives off host in an unfed state where they must resist starvation between bouts of blood feeding. Survival during these extended off‐host periods is critical to the success of these arthropods as vectors of disease; however, little is known about the underlying physiological and molecular mechanisms of starvation tolerance in ticks. We examined the bioenergetic, transcriptomic and behavioural changes of female American dog ticks,
- Award ID(s):
- 1654417
- NSF-PAR ID:
- 10330651
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 225
- Issue:
- 8
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Dermacentor variabilis , throughout starvation (up to nine months post‐bloodmeal). As starvation progressed, ticks utilized glycogen and lipid, and later protein as energy reserves with proteolysis and autophagy facilitating the mobilization of endogenous nutrients. The metabolic rate of the ticks was expectedly low, but showed a slight increase as starvation progressed possibly reflecting the upregulation of several energetically costly processes such as transcription/translation and/or increases in host‐seeking behaviours. Starved ticks had higher activity levels, increased questing behaviour and augmented expression of genes related to chemosensing, immunity and salivary gland proteins. The shifts in gene expression and associated behavioural and physiological processes are critical to allowing these parasites to exploit their ecological niche as extreme sit‐and‐wait parasites. The overall responses of ticks to starvation were similar to other blood‐feeding arthropods, but we identified unique responses that could have epidemiological and ecological significance for ticks as ectoparasites that must be tolerant of sporadic feeding. -
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Abstract Ticks are blood-feeding arthropods responsible for the transmission of disease-causing pathogens to a wide range of vertebrate hosts, including livestock and humans. Tick-borne diseases have been implicated in significant economic losses to livestock production, and this threat will increase as these obligate parasites widen their geographical ranges. Similar to other ectotherms, thermal stress due to changing global temperatures has been shown to influence tick survival and distribution. However, studies on the influence of extreme temperatures in ticks have focused on advanced, mobile stages, ignoring immobile stages that cannot move to more favorable microhabitats. In this study, low- and high-temperature regimens were assessed in relation to egg viability for hard tick species—Amblyomma maculatum (Gulf Coast tick), Ixodes scapularis (black-legged tick), Dermacentor variabilis (American dog tick), and Rhipicephalus sanguineus (Brown dog tick). Tick eggs exposed early in development (freshly laid during early embryo development) were significantly more susceptible to thermal stress when compared with those exposed later in development (late embryo development denoted by a fecal spot). Based on our studies, differences in egg hatching success among treatments were greater than in hatching success when comparing species. Lastly, there was evidence of extreme thermal exposure significantly altering the hatching times of tick eggs for specific treatments. These results provide insights into the critical period for tick egg viability in relation to thermal exposure and tick survival associated with stress and climate change.
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Miller, Samuel I. (Ed.)ABSTRACT Animals that are competent reservoirs of zoonotic pathogens commonly suffer little morbidity from the infections. To investigate mechanisms of this tolerance of infection, we used single-dose lipopolysaccharide (LPS) as an experimental model of inflammation and compared the responses of two rodents: Peromyscus leucopus , the white-footed deermouse and reservoir for the agents of Lyme disease and other zoonoses, and the house mouse Mus musculus . Four hours after injection with LPS or saline, blood, spleen, and liver samples were collected and subjected to transcriptome sequencing (RNA-seq), metabolomics, and specific reverse transcriptase quantitative PCR (RT-qPCR). Differential expression analysis was at the gene, pathway, and network levels. LPS-treated deermice showed signs of sickness similar to those of exposed mice and had similar increases in corticosterone levels and expression of interleukin 6 (IL-6), tumor necrosis factor, IL-1β, and C-reactive protein. By network analysis, the M. musculus response to LPS was characterized as cytokine associated, while the P. leucopus response was dominated by neutrophil activity terms. In addition, dichotomies in the expression levels of arginase 1 and nitric oxide synthase 2 and of IL-10 and IL-12 were consistent with type M1 macrophage responses in mice and type M2 responses in deermice. Analysis of metabolites in plasma and RNA in organs revealed species differences in tryptophan metabolism. Two genes in particular signified the different phenotypes of deermice and mice: the Slpi and Ibsp genes. Key RNA-seq findings for P. leucopus were replicated in older animals, in a systemic bacterial infection, and with cultivated fibroblasts. The findings indicate that P. leucopus possesses several adaptive traits to moderate inflammation in its balancing of infection resistance and tolerance. IMPORTANCE Animals that are natural carriers of pathogens that cause human diseases commonly manifest little or no sickness as a consequence of infection. Examples include the deermouse, Peromyscus leucopus , which is a reservoir for Lyme disease and several other disease agents in North America, and some types of bats, which are carriers of viruses with pathogenicity for humans. Mechanisms of this phenomenon of infection tolerance and entailed trade-off costs are poorly understood. Using a single injection of lipopolysaccharide (LPS) endotoxin as a proxy for infection, we found that deermice differed from the mouse ( Mus musculus ) in responses to LPS in several diverse pathways, including innate immunity, oxidative stress, and metabolism. Features distinguishing the deermice cumulatively would moderate downstream ill effects of LPS. Insights gained from the P. leucopus model in the laboratory have implications for studying infection tolerance in other important reservoir species, including bats and other types of wildlife.more » « less
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Abstract Overexpression of Arabidopsis dehydration response element binding 1a (
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.236497
