Body mass affects seasonal variation in sickness intensity in a seasonally-breeding rodent

Abstract

Species that display seasonal variation in sickness intensity show the most intense response in the season during which they have the highest body mass, suggesting that sickness intensity may be limited by an animal's energy stores. Siberian hamsters (Phodopus sungorus) display lower body masses and less intense sickness when housed in short, winter-like days as opposed to long, summer-like days. To determine whether reduced sickness intensity displayed by short-day hamsters is a product of seasonal changes in body mass, we food restricted long-day hamsters so that they exhibited body mass loss that mimicked the natural photoperiod-induced loss of body mass in short-day hamsters. We then experimentally induced sickness with lipopolysaccharide (LPS) and compared sickness responses among long-day food-restricted and long-and short-day ad libitum fed groups, predicting that long-day food-restricted hamsters would show sickness responses comparable to those of short-day ad libitum fed hamsters and attenuated in comparison to long-day ad libitum fed hamsters. We found that long-day food-restricted hamsters showed attenuated LPSinduced anorexia, loss of body mass and hypothermia compared with long-day ad libitum fed animals; however, anorexia remained elevated in long-day food-restricted animals compared with short-day ad libitum fed animals. Additionally, LPS-induced anhedonia and decreases in nest building were not influenced by body mass. Results of hormone assays suggest that cortisol levels could play a role in the attenuation of sickness in long-day food-restricted hamsters, indicating that future research should target the roles of glucocorticoids and natural variation in energy stores in seasonal sickness variation.

Neuroendocrine-immune circuits, phenotypes, and interactions

“…In house sparrows ( Passer domesticus ), glucocorticoid treatment suppresses cell-mediated immunity in birds inhabiting temperate, but not tropical, regions (Martin et al, 2005). In a reciprocal NEI interaction, plasma glucocorticoid level following bacterial lipopolysaccharide challenge is higher in Siberian hamsters ( Phodopus sungorus ) adapted to short day lengths (winter-like conditions) versus long day lengths, suggesting a photoperiodic effect (Carlton and Demas, 2015a). In tree lizards, corticosterone suppresses wound healing only during periods of energy limitation, implying a reorganization of the NEI circuit when resources are abundant (French et al, 2007).…”

“…The status of energy stores becomes more important as immune activation progresses and is conveyed through metabolic hormones, such as leptin and ghrelin (Carlton et al, 2012). Lower energy stores can lead to the termination of sickness behavior; otherwise, survival is drastically reduced once body mass (and energy stores) decreases below a minimum threshold (Ashley and Wingfield, 2012; Carlton and Demas, 2015a). …”

“…For example, there is seasonal modulation of the sickness response after bacterial lipopolysaccharide (LPS) challenge in birds and mammals (Bilbo et al, 2002; Owen-Ashley et al, 2006, 2008; Owen-Ashley and Wingfield, 2006), although there are exceptions to this rule (for e.g., Hegemann et al, 2012). This variation seems to be influenced by a combination of proximate factors that include testosterone (in males; Ashley et al, 2009), melatonin (Bilbo and Nelson, 2002), glucocorticoids (Goujon et al, 1995a, b), insulin (Carlton and Demas, 2015b) and body condition (Carlton and Demas, 2015a; Owen-Ashley et al, 2006, 2008; Owen-Ashley and Wingfield, 2006), which is partially mediated by leptin (Carlton and Demas, 2014)- a satiety hormone produced from adipose cells. From an ultimate perspective, sickness behavior represents an “opportunity cost” and thus conflicts with the expression of other activities important for reproductive and growth functions (sexual and social behavior, territorial defense, parental care, etc.…”

Glucose and insulin modulate sickness responses in male Siberian hamsters

“…Previous work has shown that food restriction results in suppression of sickness symptoms (Bilbo and Nelson, 2002; MacDonald et al, 2014; MacDonald et al, 2011). Additionally, the intensity of the energetically costly symptoms of sickness are correlated with body mass in several species, such that animals with higher body masses show more intense sickness responses (Carlton and Demas, 2015; Owen-Ashley et al, 2008; Owen-Ashley et al, 2006; Pohl et al, 2014). Siberian hamsters ( Phodopus sungorus ) are a species that shows variation in sickness intensity that correlates with energetic state.…”

“…For instance, hamsters show seasonal variation in both body mass and sickness intensity and exhibit the most intense sickness responses in the season in which they have the greatest body mass (Bilbo et al, 2002). We have previously manipulated body mass and an endocrine signal of fat stores (i.e., leptin) to determine their effects on sickness intensity variation in this species (Carlton and Demas, 2014; Carlton and Demas, 2015). These studies showed that hamsters modulate sickness symptoms in response to decreases in energy stores (i.e., attenuation of sickness-induced anorexia and body mass loss in hamsters that were food restricted to lose body mass; Carlton and Demas, 2015) and increases in circulating leptin levels (i.e., attenuation of sickness-induced hypothermia in hamsters provided exogenous leptin to simulate increased fat stores; Carlton and Demas, 2014).…”