Abstract

BackgroundLife history theory predicts that during the lifespan of an organism, resources are allocated to either growth, somatic maintenance or reproduction. Resource allocation trade-offs determine the evolution and ecology of different life history strategies and define an organisms’ position along a fast–slow continuum in interspecific comparisons. Labord’s chameleon (Furcifer labordi) from the seasonal dry forests of Madagascar is the tetrapod species with the shortest reported lifespan (4–9 months). Previous investigations revealed that their lifespan is to some degree dependent on environmental factors, such as the amount of rainfall and the length of the vegetation period. However, the intrinsic mechanisms shaping such a fast life history remain unknown. Environmental stressors are known to increase the secretion of glucocorticoids in other vertebrates, which, in turn, can shorten telomeres via oxidative stress. To investigate to what extent age-related changes in these molecular and cellular mechanisms contribute to the relatively short lifetime of F. labordi, we assessed the effects of stressors indirectly via leukocyte profiles (H/L ratio) and quantified relative telomere length from blood samples in a wild population in Kirindy Forest. We compared our findings with the sympatric, but longer-lived sister species F. cf. nicosiai, which exhibit the same annual timing of reproductive events, and with wild-caught F. labordi that were singly housed under ambient conditions.ResultsWe found that H/L ratios were consistently higher in wild F. labordi compared to F. cf. nicosiai. Moreover, F. labordi already exhibited relatively short telomeres during the mating season when they were 3–4 months old, and telomeres further shortened during their post-reproductive lives. At the beginning of their active season, telomere length was relatively longer in F. cf. nicosiai, but undergoing rapid shortening towards the southern winter, when both species gradually die off. Captive F. labordi showed comparatively longer lifespans and lower H/L ratios than their wild counterparts.ConclusionWe suggest that environmental stress and the corresponding accelerated telomere attrition have profound effects on the lifespan of F. labordi in the wild, and identify physiological mechanisms potentially driving their relatively early senescence and mortality.

Highlights

  • Life history theory predicts that during the lifespan of an organism, resources are allocated to either growth, somatic maintenance or reproduction

  • Life history theory is based on the premise that during the lifetime of an individual, energy and resources are allocated to either growth, somatic maintenance, or reproduction [1,2,3]

  • For statistical analyses (Table 3), the months June and July were excluded due to small sample sizes, and we found a negative correlation between the H/L ratio and telomere length (TL) in F. labordi ( r= − 0.556, df = 65, p < 0.01) and in F. cf. nicosiai ( r = − 0.687, df = 38, p < 0.01 ; see Fig. 3)

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Summary

Introduction

Life history theory predicts that during the lifespan of an organism, resources are allocated to either growth, somatic maintenance or reproduction. To investigate to what extent age-related changes in these molecular and cellular mechanisms contribute to the relatively short lifetime of F. labordi, we assessed the effects of stressors indirectly via leukocyte profiles (H/L ratio) and quantified relative telomere length from blood samples in a wild population in Kirindy Forest. Life history theory is based on the premise that during the lifetime of an individual, energy and resources are allocated to either growth, somatic maintenance, or reproduction [1,2,3]. In spite of the supposed significance of extrinsic factors in shaping life histories, aging research is still largely biased towards captive animals living under standardized, optimal conditions (e.g., [7]). Studies of wild populations with high extrinsic mortality are essential for testing hypotheses on the evolution of lifespan and senescence

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