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Background: Life 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., Results: We 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., Conclusion: We 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.

Among tetrapods, the current record holder for shortest lifespan is Labord's chameleon, Furcifer labordi. These reptiles from the arid southwest of Madagascar have a reported lifespan of 4-5 months during the annual rainy season and spend the majority of their life (8-9 months) as a developing embryo. This semelparous, annual life history is unique among tetrapods, but only one population (Ranobe) in the southernmost distribution range has been studied. We therefore investigated the potential for environmentally-dependent variability in lifespan in a population in Kirindy Forest, which has a much longer warm rainy season. While no adults were found after March in Ranobe, the disappearance of adults was delayed by several months in Kirindy. Our data also revealed sex-biased mortality, suggesting that females have a longevity advantage. Furthermore, we found that, after an unusually long previous rainy season, one female was capable of surviving until a second breeding season. Keeping F. labordi in cages under ambient conditions demonstrated that also males can also survive until the next season of activity under these conditions. Our study therefore revealed considerable variability in the extreme life history of this tetrapod that is linked to variation in ecological factors.