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Senescence in an Annual Reptile, Labord's Chameleon

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Senescence in an Annual Reptile, Labord's Chameleon A short story: senescence in an annual reptile, Labord’s chameleon (Furcifer labordi) Dissertation for the award of the degree "Doctor rerum naturalium" (Dr.rer.nat.) of the Georg-August-Universität Göttingen Within the doctoral program GAUSS Basic Program in Biology of the Georg-August University School of Science (GAUSS) Submitted by Falk Eckhardt Born in Duisburg, Germany Göttingen, 2019 Thesis Committee Prof. Dr. Peter Kappeler, Department of Sociobiology/Anthropology, Georg-August- University of Göttingen Prof. Dr. Stefan Scheu, J.F. Blumenbach Institute of Zoology and Anthropology, Department of Animal Ecology, University of Göttingen, Göttingen PD. Dr. Matthias Waltert, Department of Conservation Biology/Workgroup on Endangered Species, Georg-August-University of Göttingen Members of the Examination Board First Reviewer: Prof. Dr. Peter Kappeler, Department of Sociobiology/Anthropology, Georg-August- University of Göttingen Second Reviewer: Prof. Dr. Stefan Scheu, J.F. Blumenbach Institute of Zoology and Anthropology, Department of Animal Ecology, University of Göttingen Further members of the Examination Board Dr. Sven Bradler, J.F. Blumenbach Institute of Zoology and Anthropology, Department of Animal Ecology, University of Göttingen, Göttingen Prof. Dr. Eckhard Heymann, Department of Sociobiology/Anthropology, Georg-August- University of Göttingen Prof. Dr. Christina Strube, Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Hannover PD. Dr. Matthias Waltert, Department of Conservation Biology/Workgroup on Endangered Species, Georg-August-University of Göttingen Date of the oral examination: 11.12.2019 CONTENTS Summary 1 Zusammenfassung 4 Chapter 1 7 General Introduction 7 Why do we age? 8 How variable is senescence? 10 Aging under natural versus protected conditions 13 Semelparity 16 Study species: The Labord’s chameleon Furcifer labordi (Grandidier, 1872) 18 Study aims and approaches 19 Chapter 2 21 Highly variable lifespan in an annual reptile, Labord’s chameleon (Furcifer labordi) Chapter 3 30 Life-histories, demographies and population dynamics of three sympatric chameleon species (Furcifer spp.) from western Madagascar Chapter 4 52 Parasite burden in a short-lived chameleon, Furcifer labordi Chapter 5 74 Stress-related changes in leukocyte profiles and telomere shortening in the shortest-lived tetrapod, Furcifer labordi. Chapter 6 91 General Discussion 91 Intraspecific, interannual and intersexual differences in the lifespan of F. labordi 91 Lifespan of F. labordi in captivity 94 Interspecific comparison and life-histories of chameleons 95 Intrinsic mechanisms of senescence in F. labordi 99 Potential of aging research in reptiles 102 Conclusion 104 References 106 Acknowledgement 137 List of figures 138 List of tables 139 Curriculum vitae 140 Publications 141 Declaration 142 Summary Among animals, the fast-slow continuum is the dominant axis that shapes life-history variation. As resources are limited a trade-off occurs between a short lifespan, young age at maturity, high reproductive rates and high aging rates or the other way round. At an ultimate level, rates of adult mortality with age are assumed to determine whether a species falls in the one or in the other continuum, at which high rates of extrinsic mortality select for fast life-histories. Within terrestrial vertebrates (tetrapods), the current record holder for short lifespan is the Labord’s chameleon, Furcifer labordi. These chameleons, inhabiting the seasonal western and southwestern deciduous dry forests of Madagascar, were found to have a post-hatching lifespan of only several months. At the onset of the active respectively rainy season, in November, a cohort of hatchlings emerges. Their early life is determined by rapid growth, resulting in fast sexual maturity and subsequent reproduction in January-February. After the mating season, senescent declines become apparent, and at the beginning of the dry season, a fast die-off has been observed in both sexes. Hereafter, the population only exists as eggs, probably as an adaption to survive the harsh dry season. High adult mortality combined with relatively high juvenile (here egg) survival might have ultimately selected for this annual life-history. It is unique in tetrapods and makes this chameleon an intriguing model species for investigating the proximate and ultimate factors shaping rapid senescence, especially because perennial, sympatric congeners are available for comparative studies. Semelparity, i.e. the strategy to allocate all energy in one reproduction event, is rarely found in tetrapods and has apart from a very few reptile species only been detected in a few small-sized marsupial species. However, in these marsupial species the die-off following the mating season is restricted to males, while several females survive until the next breeding season. Apart from these species, for which the male die-off is obligate, less extreme cases of semelparity have been documented. Here, facultative male die-off is restricted to some populations and/or only observed in some years and has been linked to variable resource availability. Strong prey seasonality that leads to a short breeding season has been suggested to explain male semelparity in marsupials, at which high levels of sperm competition combined with female reproductive synchrony select for obligate semelparity. Interestingly, males that were captured before engaging in reproductive season, can survive for more than two years. However, while captivity may shield males from early death due to extrinsic factors, they still experience loss in body mass and irreversible regression of sexual organs as observed in their wild conspecifics after the mating season, proposing an annual, intrinsic pacesetter. In contrast 1 to these marsupials, the proximate causes leading to the short life in this chameleon species remain entirely unknown. Is it the consequence of extrinsic factors, such as intense intra-sexual competition, high predation rates, and low food availability, or are the physiological changes leading to rapid senescence internally “programmed” and thus impending? In the marsupials mentioned above, both factors seem to play a role. Furthermore, so far, only one population in the southernmost and thus driest distribution range of this species has been studied in detail. Thus, the ultimate aim of my thesis is to reflect on the interplay between the external and internal factors that favour the short life-history of this chameleon species. In the first study, I investigated the variability of lifespan in a population of F. labordi in the Kirindy Forest, which has a much longer rainy season compared to the more southern habitat. I documented that the population wide die-off is prolonged in Kirindy several months forward. Moreover, I showed a bias in sex-specific mortality, in which females have a longevity advantage. To exclude most extrinsic factors of mortality, I kept several individuals in captivity and demonstrated that both sexes could survive until the next season of activity. Therefore, this study revealed considerable plasticity of this life-history that is associated to differences in ecological factors. Within the second study, I compared the life-history of F. labordi with those of the congeneric and sympatric species F. cf. nicosiai and F. oustaleti in the Kirindy forest and tested for potential niche segregation that might have driven evolutionary selection for this short lifespan. In all three species, I found high interspecific differences in time of hatching, growth rates, age at reproduction, adult body size and lifespan. While the cohort of F. labordi was already adult, hatchlings of the F. oustaleti and subsequently F. cf. nicosiai emerged. As hatchlings in these species are similar-sized, these differences indicate dietary niche segregation. However, I found that compared to other similar sized lizards, the lifespans of F. cf. nicosiai and F. oustaleti are considerably short and probably attributed to the ecology of chameleons. In the third study, I examined to which extend parasite infection as a proxy of overall health in F. labordi might be connected to the short lifespan. Therefore, I inspected gastrointestinal, - blood - and ectoparasite burden and compared my findings to those of the sympatric and longer living F. cf. nicosiai and the caged individuals. Within F. labordi, I found an intense increase of prevalence in gastrointestinal parasites over the reproductive period. Males showed a higher prevalence that could be caused by frequent male-male combats resulting in higher baseline stress levels and their earlier disappearance. Contrary to our expectations, gastrointestinal, - blood - and ectoparasite burden was higher in adult F. cf. nicosiai. In captivity, both sexes showed less parasite burden and were longer living than their wild conspecifics. The final study aimed at determining the effect of glucocorticoids (GCs) and 2 telomere shortening as well as their interplay on the acceleration of the aging process in F. labordi. To indirectly measure baseline stress levels, I used the ratio between heterophils to lymphocytes (H/L ratio) in blood smears as an indicator of physiological stress since a rise in GC level is closely correlate with a decrease in lymphocytes and increase of heterophils. I quantified telomere length using real-time quantitative PCR (qPCR) in relative telomere length (TL) in blood cells. I found that H/L ratios were higher in wild F. labordi
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