Eating when ill is risky: immune defense impairs food detoxification in the caterpillar,Manduca sexta

Abstract

Mounting an immune response consumes resources, which should lead to increased feeding. However, activating the immune system reduces feeding (i.e. illness-induced anorexia) in both vertebrates and invertebrates, suggesting that it may be beneficial. We suggest that illness-induced anorexia may be an adaptive response to conflicts between immune defense and food detoxification. We found that activating an immune response in the caterpillar increased its susceptibility to the toxin permethrin. Conversely, a sublethal dose of permethrin reduced resistance to the bacterium, demonstrating a negative interaction between detoxification and immune defense. Immune system activation and toxin challenge each depleted the amount of glutathione in the hemolymph. Increasing glutathione concentration in the hemolymph increased survival for both toxin- and immune+toxin-challenged groups. The results of this rescue experiment suggest that decreased glutathione availability, such as occurs during an immune response, impairs detoxification. We also found that the expression of some detoxification genes were not upregulated during a combined immune-toxin challenge, although they were when animals received a toxin challenge alone. These results suggest that immune defense reduces food detoxification capacity. Illness-induced anorexia may protect animals by decreasing exposure to food toxins when detoxification is impaired.

Malpighamoebainfection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

“…Both their immune system and their ability to detoxify noxious food substances rely on pathways that involve the antioxidant glutathione (Habig et al ., 1974; Stahlschmidt et al ., 2015; Jeschke et al ., 2016). Consequently, competition for glutathione between these two physiological pathways could lead to impaired detoxification when the immune system is already activated (McMillan et al ., 2018). Whether due to a direct reduction in feeding or as an indirect consequence of a trade-off with the immune response, reduced food intake lowers the risk of ingesting toxins but also prevents locusts acquiring water and nutrients.…”

“…Alaux et al ., 2010; Vidau et al ., 2011), suggest that pesticide exposure can exacerbate the effects of pathogens. Moreover, pathogens may themselves exacerbate the impacts of xenobiotics, possibly due to trade-offs between the activity of the immune system and detoxification pathways (McMillan et al ., 2018). In most cases, the mechanisms linking the susceptibly of insects to xenobiotics with the presence of pathogens remain unknown, even in the case of diseases of insect pollinators that provide commercially-important ecosystem services (reviewed in Goulson et al ., 2015).…”

Pollen Alters Amino Acid Levels in the Honey Bee Brain and This Relationship Changes With Age and Parasitic Stress

“…Cysteine, for example, was the amino acid whose concentration was most affected by pollen in our study. Cysteine is a limited resource in most insects, and necessary for glutathione production, an antioxidant found to neutralize reaction oxygen species and support immune function (McMillan et al, 2017). Tyrosine, another amino acid found to alter with pollen and infection is directly involved in protein phosphorylation, nitrosation, and sulfation; and is a precursor for dopamine: a neurotransmitter in the honey bee brain involved in behaviors like learning and memory (Agarwal et al, 2011).…”

Friend or foe? Effects of host immune activation on the transient gut microbiome in the caterpillarManduca sexta

“…Another potential reason to remove the microbiome is that having to regulate it requires immune 85 resources in insects (Zhai et al, 2018) These costs could be problematic when M. sexta is facing 86 multiple stressors simultaneously. Facing a combination of predators, toxins, or pathogens leads 87 to a significantly increased likelihood of mortality than if each challenge was faced 88 alone (McMillan et al, 2018). The increased mortality is due, in part, to physiological trade-offs 89 between different defense systems (e.g.…”

“…A third possibility is that resource limitation may produce a reconfiguration of physiological 119 networks as opposed to straightforward trade-offs. In some situations, M. sexta larvae adopt an 120 alternate network configuration when faced with dual challenges (Adamo et al, 2016a;Adamo 121 et al, 2017;McMillan et al, 2018). These alternative network strategies take the pressure off of 122 molecular pinch points and increase survival (Adamo et al, 2016b;Adamo et al, 2017;123 McMillan et al, 2018).…”