The effect of hydration state and energy balance on innate immunity of a desert reptile

Abstract

IntroductionImmune function is a vital physiological process that is often suppressed during times of resource scarcity due to investments in other physiological systems. While energy is the typical currency that has been examined in such trade-offs, limitations of other resources may similarly lead to trade-offs that affect immune function. Specifically, water is a critical resource with profound implications for organismal ecology, yet its availability can fluctuate at local, regional, and even global levels. Despite this, the effect of osmotic state on immune function has received little attention.ResultsUsing agglutination and lysis assays as measures of an organism’s plasma concentration of natural antibodies and capacity for foreign cell destruction, respectively, we tested the independent effects of osmotic state, digestive state, and energy balance on innate immune function in free-ranging and laboratory populations of the Gila monster, Heloderma suspectum. This desert-dwelling lizard experiences dehydration and energy resource fluctuations on a seasonal basis. Dehydration was expected to decrease innate immune function, yet we found that dehydration increased lysis and agglutination abilities in both lab and field studies, a relationship that was not simply an effect of an increased concentration of immune molecules. Laboratory-based differences in digestive state were not associated with lysis or agglutination metrics, although in our field population, a loss of fat stores was correlated with an increase in lysis.ConclusionsDepending on the life history of an organism, osmotic state may have a greater influence on immune function than energy availability. Thus, consideration of osmotic state as a factor influencing immune function will likely improve our understanding of ecoimmunology and the disease dynamics of a wide range of species.

Dehydration enhances multiple physiological defense mechanisms in a desert lizard, Heloderma suspectum

“…Our immune response results verify our previous findings that dehydration enhances agglutination and lysis in the Gila monster (Moeller et al, 2013). Additionally, using captive animals, we show that another estimate of innate immune response, bacterial killing ability, also increases with dehydration in this species.…”

“…However, if this were the case, one would expect to find a decrease in immune function in dehydrated Gila monsters, as prolonged exposure to glucocorticoids like CORT usually inhibits immune function (Sapolsky et al, 2000; though there are exceptions, see Martin et al, 2011). Thus, contrary to the trend, but in accordance with our previous result of enhanced innate immune function in dehydrated Gila monsters (Moeller et al, 2013), we predicted that initial levels of CORT would not be affected by Fig. 3.…”

“…Interestingly, however, a glucocorticoid response to dehydration is lacking in Children's pythons (Antaresia childreni; Dupoué et al, 2014), Awassi sheep (Ovis aries; Jaber et al, 2004;Hamadeh et al, 2006; but see Ghanem et al, 2008) and humans (Homo sapiens; Malarkey et al, 1993;Hoffman et al, 1994; but see Maresh et al, 2006). Similarly, the negative relationship between dehydration and immune function is also not without exception, as we have demonstrated that Gila monsters, Heloderma suspectum, have improved innate immune performances when dehydrated (Moeller et al, 2013). Unfortunately, the interplay of the three components of this relationship (dehydration, the stress response and immunity) has not been studied in a single species.…”

“…Thus energetically cheaper innate immunity may increase instead as a strategy to limit vulnerability of the immune system, although this hypothesis remains untested. The mechanisms by which dehydration increases innate immune function also warrant further study, as it was previously shown that increased plasma concentration of immune molecules is not the sole cause (Moeller et al, 2013). We posit that this response of the immune and endocrine systems to dehydration, which goes against the general expected pattern, may be an adaptation of species that regularly experience bouts of dehydration.…”

“…We collected blood samples from captive and free-ranging Gila monsters in hydrated and dehydrated states to: (1) test the repeatability of our previous findings of increased innate immunity (i.e. hemolysis and hemagglutination tests; Moeller et al, 2013) during moderate dehydration, (2) examine additional measures of innate immunity including bacterial killing ability and white blood cell differential, and (3) determine plasma corticosterone (CORT, the natural glucocorticoid of reptiles) concentrations prior to and after a stress perturbation in multiple hydration states. Comparing measures of initial CORT during the hydrated and dehydrated states will inform us as to whether dehydration can be viewed as a direct stressor, while the post-perturbation measure of CORT tests whether dehydrated animals exhibit elevated stress responsiveness to their surroundings.…”