Immune Profile Predicts Survival and Reflects Senescence in a Small, Long-Lived Mammal, the Greater Sac-Winged Bat (Saccopteryx bilineata)

Abstract

The immune system imposes costs that may have to be traded against investment of resources in other costly life-history traits. Yet, it is unknown if a trade-off between immunity and longevity occurs in free-ranging mammals. Here, we tested if age and survival, two aspects associated with longevity, are linked to immune parameters in an 8 g bat species. Using a combination of cross-sectional and longitudinal data, we assessed whether total white blood cell (WBC) counts, bacterial killing ability of the plasma (BKA) and immunoglobulin G (IgG) concentration change with age. Furthermore, we asked if these immune parameters impose costs resulting in decreased survival probabilities. We found that WBC counts decreased with age both within and among individuals. IgG concentrations were higher in older individuals, but did not change with age within individuals. Furthermore, individuals with above average WBC counts or IgG concentration had lower probabilities to survive the next six months. High WBC counts and IgG concentrations may reflect infections with parasites and pathogens, however, individuals that were infected with trypanosomes or nematodes showed neither higher WBC counts or IgG concentrations, nor was infection connected with survival rates. BKA was higher in infected compared with uninfected bats, but not related to age or survival. In conclusion, cellular (WBC) and humoral (IgG) parts of the immune system were both connected to age and survival, but not to parasite infections, which supports the hypothesis that energetically costly immunological defences are traded against other costly life-history traits, leading to a reduced lifespan in this free-ranging mammal.

Immunosenescence in wild animals: meta‐analysis and outlook

“…Depicted are phylogenetic relatedness on the left, scientific names for all species included (blue = data collected in wild population, red = data collected in captive population), and for each species the number of effects in each main component of the immune system and the relevant references. References: 1: (Lindsay et al ); 2: (Beirne et al ); 3: (Mazzaro et al ); 4: (Mellish et al ); 5: (Schneeberger et al ); 6: (Cheynel et al ); 7: (Graham et al ); 8: (Nussey et al ); 9: (Watson et al ); 10: (Grandoni et al ); 11: (Ezenwa & Jolles ); 12: (Ahmad et al ); 13: (Abolins et al ); 14: (Nehete et al ); 15: (Nehete et al ); 16: {Castro:2015hz}; 17: (Cicin‐Sain et al ); 18: (Čičin‐Šain et al ); 19: (Coe & Ershler ); 20: (Coe et al ); 21: (Ershler et al ): 22: (Higashino et al ): 23: (Eichberg et al ); 24: (Jayashankar et al ); 25: (Setchell et al ); 26: (Chakrabarti et al ); 27: (Sharma et al ); 28: (Massot et al ); 29: (Richard et al ); 30: (Madsen et al ); 31: (Ujvari & Madsen ); 32: (Ujvari & Madsen ); 33: (Sparkman & Palacios ); 34: (Zimmerman et al ); 35: (Zimmerman et al ); 36: (Zimmerman et al ); 37: (Groffen et al ); 38: (Lavoie et al ); 39: (Alonso‐Alvarez et al ); 40: (Hill et al ); 41: (Counihan & Hollmén ); 42: (Neggazi et al ); 43: (Terrón et al ); 44: (Apanius & Nisbet ); 45: (Lozano & Lank ); 46: (Lozano & Lank ); 47: (Nebel et al ); 48: (Torres & Velando ); 49: (Haussmann et al ); 50: (Lecomte et al ); 51: (Catry et al ); 52: (Wilcoxen et al ); 53: (Vermeulen et al ); 54: (Møller & Haussy ); 55: (Saino et al ); 56: (Palacios ...…”

Anthropogenic food provisioning and immune phenotype: Association among supplemental food, body condition, and immunological parameters in urban environments

“…). Similarly, previous studies interpreted increased IgG concentration as a sign of chronic infection or accumulation of repeated pathogen exposure (Brock et al., ; Schneeberger et al., ). Although extreme malnutrition may hinder production of IgG (Frouin, Haulena, Akhurst, Raverty, & Ross, ; Glick, Day, & Thompson, ), this is less likely to apply in our study, as overall cats showed similarly moderate body condition regardless of the CCA intensity.…”

“…Similar energetic trade‐offs among different immune components have been discussed and observed in previous studies (Martin, Weil, Kuhlman, & Nelson, ; Pigeon, Bélisle, Garant, Cohen, & Pelletier, ). For instance, in a study of different bat colonies, bats in areas potentially exposed to fungi and parasites in higher rate, hence requiring stronger memory‐related resistance, showed higher T‐cell‐mediated immune responses while their bactericidal ability was lower, showing negative correlation between the two immune parameters (Allen et al., ; Brock et al., ; Schneeberger et al., ).…”

“…Based on the effect of corticosteroid stress hormone on reducing number of lymphocyte while increasing neutrophils in multiple vertebrate taxa, N:L ratio is considered a reliable marker for glucocorticoid levels (Davis, Maney, & Maerz, ) and has been applied in previous studies as index of stress (Bosson, Islam, & Boonstra, ; Johnstone, Lill, & Reina, ). We measured two humoral immune parameters: the bacterial killing assay (BKA) and total immunoglobulin G (IgG) concentration as indicators of innate and adaptive immune defenses, respectively (Lee, ; Schneeberger, Courtiol, Czirják, & Voigt, ). Specifically, BKA against E. coli and S. aureus characterizes functionally relevant actions of complement proteins and natural antibodies, a reflection of innate immunity (French et al., ).…”

Social effects on age-related and sex-specific immune cell profiles in a wild mammal

“…The immune system involves multiple mechanisms that protect the host against pathogens [1]. The 33 functioning of the immune system is related to sex [2,3] and changes throughout life [4][5][6][7][8][9]. Since age-34 related changes in immune responses have been linked to mortality in the wild [9], understanding the 35 factors driving differences in immune responses can provide insight into the evolution of immunity 36 and senescence.…”