The stress of growing old: sex- and season-specific effects of age on allostatic load in wild grey mouse lemurs

Abstract

Chronic stress [i.e. long-term elevation of glucocorticoid (GC) levels] and aging have similar, negative effects on the functioning of an organism. Aged individuals' declining ability to regulate GC levels may therefore impair their ability to cope with stress, as found in humans. The coping of aged animals with long-term natural stressors is virtually unstudied, even though the ability to respond appropriately to stressors is likely integral to the reproduction and survival of wild animals. To assess the effect of age on coping with naturally fluctuating energetic demands, we measured stress hormone output via GC metabolites in faecal samples (fGCM) of wild grey mouse lemurs (Microcebus murinus) in different ecological seasons. Aged individuals were expected to exhibit elevated fGCM levels under energetically demanding conditions. In line with this prediction, we found a positive age effect in the dry season, when food and water availability are low and mating takes place, suggesting impaired coping of aged wild animals. The age effect was significantly stronger in females, the longer-lived sex. Body mass of males but not females correlated positively with fGCM in the dry season. Age or body mass did not influence fGCM significantly in the rainy season. The sex- and season-specific predictors of fGCM may reflect the differential investment of males and females into reproduction and longevity. A review of prior research indicates contradictory aging patterns in GC regulation across and even within species. The context of sampling may influence the likelihood of detecting senescent declines in GC functioning.

Allostatic load and biological anthropology

“…Additionally, those who responded to social reorganization with larger increases in cortisol were at greater risk for infection (Cohen et al, 1997). example, great apes and humans share a propensity to cardiomyopathy (Hansen, Alford, & Keeling, 1984) and heart failure, the leading cause of death in great apes (Videan et al, 2009 (Pryce, Dettling, Spengler, Schnell, & Feldon, 2004), mentioned in the introduction of reports (F€ urtbauer, Heistermann, Sch € Ulke, & Ostner, 2014;Hämäläinen, Heistermann, & Kraus, 2015;Hoffman et al, 2011;Laudenslager, Jorgensen, & Fairbanks, 2012;MacIntosh, Alados, & Huffman, 2011;MacLarnon et al, 2015;Schoof, Jack, & Ziegler, 2014), and/or used to frame results in discussions (Coplan et al, 2015;Barr, Newman, Lindell, et al, 2004;F€ urtbauer et al, 2014;Hoffman et al, 2011;MacIntosh et al, 2011;Mendonça-Furtado et al, 2014;Onyango, Gesquiere, Wango, Alberts, & Altmann, 2008 ( variety of publications. One group assigned allostatic load levels to various animal species based on dominance rank without calculating an ALI (Goymann & Wingfield, 2004 ACTH, adrenocorticotropin-releasing hormone; BMI, body mass index; CRF, corticotropin-releasing factor; DBP, diastolic blood pressure; DHEA-S, dehydroepiandrosterone-sulfate; HDL, high-density lipoprotein; IGF-1, insulin-like growth factor 1; IL-1ra, interleukin-1 receptor antagonist; IL-6, interleukin-6; IL-8, interleukin-8; LDL, low-density lipoprotein; LH, luteinizing hormone; SBP, systolic blood pressure; WBC, white blood cells.…”

“…Only since 2004 have allostasis theory or allostatic load been referenced in any primate journals. For example, allostasis and/or allostatic load have been listed as keywords (Pryce, Dettling, Spengler, Schnell, & Feldon, 2004), mentioned in the introduction of reports (F€ urtbauer, Heistermann, Sch € Ulke, & Ostner, 2014;Hämäläinen, Heistermann, & Kraus, 2015;Hoffman et al, 2011;Laudenslager, Jorgensen, & Fairbanks, 2012;MacIntosh, Alados, & Huffman, 2011;MacLarnon et al, 2015;Schoof, Jack, & Ziegler, 2014), and/or used to frame results in discussions (Coplan et al, 2015;Barr, Newman, Lindell, et al, 2004;F€ urtbauer et al, 2014;Hoffman et al, 2011;MacIntosh et al, 2011;Mendonça-Furtado et al, 2014;Onyango, Gesquiere, Wango, Alberts, & Altmann, 2008 (Goymann & Wingfield, 2004). Referring to this as the "allostasis model of dominance rank," some primatologists have referenced it in their studies of dominance hierarchies (Le Roux, Beehner, & Bergman, 2011;Mendonça-Furtado et al, 2014) and Setchell, Smith, Wickings, and Knapp (2008) used this approach in a study on sociality, testosterone, and ornamentation in male mandrills (Mandrillus sphinx).…”

Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar

“…The dry season in Kirindy Forest is accompanied by energetically demanding conditions for lemurs due to reduced availability of resources like insects, fruit and leaves, which may reduce body condition (Lewis and Kappeler, 2005;Hämäläi-nen et al, 2014). In addition, an increase of fecal glucocorticoid metabolites has been found in M. murinus in the dry season, reflecting higher levels of stress (Hämäläinen et al, 2015a). Thus, immune function may be impaired in the dry season due to a trade-off in resource allocation with other body functions (Sheldon and Verhulst, 1996;Martin et al, 2008) and/or due to the immunosuppressive effects of chronically elevated glucocorticoid hormones (Webster Marketon and Glaser, 2008;Cohen et al, 2012).…”

Conservation implications of a lack of relationship between baseline glucocorticoids and fitness in a wild passerine

“…, Hämäläinen et al. ) could influence our ability to detect a GC–fitness relationship, if fine‐scale age metrics are necessary (i.e., if pooling age categories will mask a relationship between GCs and fitness), this will limit the application of the technique in many species of concern that are not easily aged in a field setting.…”

“…We were therefore only able to partition birds into two age categories: (1) less than or equal to one year old, or (2) equal to/greater than two years, potentially encompassing ages of 2-12 years ) and as such, a range of potential brood values. While the possibility remains that age-related changes in baseline GCs (Angelier et al 2006, Mateo 2006, Riechert et al 2012, Hämäläinen et al 2015 could influence our ability to detect a GC-fitness relationship, if fine-scale age metrics are necessary (i.e., if pooling age categories will mask a relationship between GCs and fitness), this will limit the application of the technique in many species of concern that are not easily aged in a field setting.…”