Elevated neopterin levels in wild, healthy chimpanzees indicate constant investment in unspecific immune system

Verena Behringer,Klaus Zuberbühler,Fabian H Leendertz,Catherine Crockford,Roman M Wittig,Tobias Deschner,Jeroen M G Stevens

doi:10.1186/s40850-019-0041-1

Abstract

BackgroundEcological immunology proposes that the optimal immune defence, and the costs coming with it, vary across environments. In environments with higher pathogen load, the immune system should experience greater challenges and, therefore, investment in maintaining it should be higher. The biomarker neopterin allows monitoring of innate immune responses, and is therefore an ideal tool to investigate the effects of ecological variables on the immune system. Here, we compared urinary neopterin levels of apparently healthy chimpanzees without acute symptoms of sickness across two environments: in captivity (22 zoos) and in the wild (two populations).ResultsOur results revealed that urinary neopterin levels were nearly twice as high in wild compared to captive chimpanzees, independent of chimpanzee subspecies.ConclusionWe conclude that wild chimpanzees experience more frequent immune challenges in comparison to captive individuals. Therefore, wild individuals have to allocate more energy to immune function and away from reproduction and growth. Our data indicate that the generally delayed development of wild animals in comparison to captive individuals might not only be related to lower energy intake but might result from greater energy allocations to immune function. Finally, our data highlight the importance of understanding immune costs for accurate characterization of energy budgets in animals.

Highlights

Ecological immunology proposes that the optimal immune defence, and the costs coming with it, vary across environments
To evaluate the impact of immune system challenges in different environments, we investigated patterns of urinary neopterin levels as a measure for the unspecific immune response in chimpanzees living in 22 zoos and in two natural environments
The full/null model comparison (χ2 = 28.608, df = 8, P < 0.001) revealed that the environment was a significant predictor of urinary neopterin levels (Table 2), with significant lower urinary neopterin levels in captive chimpanzees in comparison to wild living individuals

Summary

Introduction

Ecological immunology proposes that the optimal immune defence, and the costs coming with it, vary across environments. The biomarker neopterin allows monitoring of innate immune responses, and is an ideal tool to investigate the effects of ecological variables on the immune system. Life-history theory (LHT) concepts show the demands and challenges that influence immune function in an ecological context. Not fully developed in neonates, innate immunity develops faster than adaptive immunity. Such defences include both physical barriers and biochemical factors—e.g., anatomical and physiological barriers, inflammatory mediators, and cellular components [8]. Neopterin is an ideal marker to monitor the (2019) 4:2 degree of the innate immune response activation [9, 10]. Increases in neopterin concentrations in serum during the clinical course of infections are paralleled by the same patterns in urine [15], and the measurement of urinary neopterin levels in non-human primates with a commercial neopterin assay has been recently validated [16, 17]

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