When Do We Eat? The Clock is Ticking

Ticks are simultaneously fascinating and disgusting. Anyone who has removed a bloated blood‐filled tick from themselves or a pet understands the “yuck“ factor they arouse. But ticks are also fascinating from a physiological perspective. Ticks are the ultimate sit‐and‐wait predators. Female ixodid ticks (hard ticks) consume a single meal during each life stage (larva, nymph and adult), which means only three lifetime meals over a 1‐ to 3‐year lifespan. Most males do not feed as adults, so they only feed twice. Thus, prolonged starvation is a quintessential aspect of tick life history. Although ticks have been widely studied for their importance as disease vectors, the vast majority of research has focused on tick–host interactions. Ixodid ticks spend the overwhelming majority of their lives off their hosts, but little is known about these periods. A new study begins to fill in some of these knowledge gaps. In this issue of Molecular Ecology, Rosendale, Dunlevy, Marshall, and Benoit examine physiological, behavioural and transcriptomic changes occurring during long‐term starvation of the American dog tick, Dermacentor variabilis. Their work provides insights into how ticks are able to go so long between meals and how they prepare for their next meal.


Abstract
Ticks are simultaneously fascinating and disgusting. Anyone who has removed a bloated blood-filled tick from themselves or a pet understands the "yuck" factor they arouse. But ticks are also fascinating from a physiological perspective. Ticks are the ultimate sit-and-wait predators. Female ixodid ticks (hard ticks) consume a single meal during each life stage (larva, nymph and adult), which means only three lifetime meals over a 1-to 3-year lifespan. Most males do not feed as adults, so they only feed twice.
Thus, prolonged starvation is a quintessential aspect of tick life history. Although ticks have been widely studied for their importance as disease vectors, the vast majority of research has focused on tick-host interactions. Ixodid ticks spend the overwhelming majority of their lives off their hosts, but little is known about these periods. A new study begins to fill in some of these knowledge gaps. In this issue of Molecular Ecology, Rosendale, Dunlevy, Marshall, and Benoit examine physiological, behavioural and transcriptomic changes occurring during long-term starvation of the American dog tick, Dermacentor variabilis. Their work provides insights into how ticks are able to go so long between meals and how they prepare for their next meal.
substantially, but quantitatively contributed only a minor amount to metabolism. Instead, long-term starvation appeared to be fuelled by protein catabolism. Molecular data described below support this idea.
The physiological and behavioural data reveal that ticks are not just sitting-and-waiting between meals, but are changing over time. Rosendale et al. (2018) used RNA-seq to generate whole-tick transcriptomes up to 36 weeks post-moult, when significant mortality began to set in. The first problem to be addressed was that the genome of D. variabilis has not been sequenced, and existing tick ge- gland genes were selected to determine whether ticks might prepare for feeding during long-term starvation, even before they detect a host.
Previous studies had suggested that at least some ticks catabolize proteins between meals; this study confirms this for dog ticks and finds supporting molecular evidence. Over 300 autophagyrelated contigs were differentially expressed during starvation.
Of special interest were seven that were directly involved in autophagy (as opposed to regulation of the process). Two of these increased rapidly in expression from Week 1 to Week 7, while the other five showed consistent increases in expression through 36 weeks. Overall, changes in autophagy-related gene expression, as well as decreases in peptidase inhibitors, were consistent with protein catabolism during starvation, suggesting that this is part of the normal tick starvation response.
While gustatory receptors did not change in expression, 5 of 19 contigs annotated as ionotropic receptors did. Although these expression differences could be somewhat inconsistent, three of the putative ionotropic receptors were most highly expressed after 36 weeks of starvation. If these are indeed related to host detection, these changes in gene expression are consistent with the increased questing behaviour as starvation continues. More consistent patterns were noted for immune function and salivary gland genes.
Both categories showed generally increased expression as starvation progressed. These changes suggest a progressive readiness for consuming their next meal.
The picture emerging from this study is one of relatively slow changes during long-term starvation. Ticks are not in stasis until the next meal literally walks by, but are making physiological adjustments over time. They switch to protein catabolism as lipid reserves decline, they become more proactive in their foraging behaviours, and they prepare biochemically to consume their next meal. These patterns are consistent with the observed transcriptome changes, but much remains to be done. Rosendale et al. used