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Sex-specific aging: Sex differences in survival and health in a wild primate population

dc.contributor.advisorKappeler, Peter M. Prof. Dr.
dc.contributor.authorHämäläinen, Anni
dc.titleSex-specific aging: Sex differences in survival and health in a wild primate populationde
dc.contributor.refereeKappeler, Peter M. Prof. Dr.
dc.description.abstractengAgeing influences the functioning of most living organisms in myriad ways and has profound consequences for their reproductive fitness and survival. Age-related changes in the functioning of an organism are thought to result from the weakened selection against deleterious mutations acting after the peak reproductive age, and selection optimizing resource allocation to reproduction versus self-maintenance. Consequently, life history theory predicts that the rate of senescence should be reduced and the age of onset of senescence delayed with increasing lifespan. A high risk of mortality from extrinsic causes should lead to earlier or faster senescence. Extensions of this theory lead to the prediction that the shorter-lived sex (e.g. males in most mammals) should show earlier senescence. Furthermore, the sex-specific selective pressures for lifespan and reproductive rate might be expected to lead to a preferential maintenance of traits that optimize immune function and self-maintenance in females, whereas male fitness may be better enhanced by a prolonged investment in competitive ability. Senescent declines might thus be expected to show trait- and sex-specific patterns. However, beyond comparative studies of age-related mortality rates, these predictions remain largely untested under natural conditions. The aim of this thesis was to test these elemental predictions by studying sex-specific functional senescence (within-individual deterioration in physiological or physical functioning) in a sexually monomorphic, small-bodied primate species (gray mouse lemur, Microcebus murinus) that experiences a high risk of extrinsic mortality in its natural environment. To gain an understanding of the prevalence of senescence across traits, and how this is influenced by selective mortality of individuals in poor condition, I examined sex-specific age trajectories in four different components of health that together broadly indicate the overall functioning of the individual and its ability to cope with environmental demands: body mass, physical strength, gastrointestinal parasite burden and allostatic load (baseline glucocorticoid level). To estimate the significance of selective disappearance and for quantifying body mass senescence, I used long-term data (10-18 generations) from a captive breeding colony in Brunoy, France, and two wild populations in Kirindy, western Madagascar. I collected grip strength measurements and fecal samples over two dry and two rainy seasons from a long-term monitored, individually marked wild gray mouse lemur population. To compare the patterns of senescence between wild and captive animals, I additionally measured grip strength of captive animals. In the first study, selective disappearance of individuals with declining body mass was found in both, the captive and wild setting, whereas a senescent decline in the ability to regain lost body mass was found only in captivity. Some evidence was found that mortality in the wild was more condition-dependent in females than in males, and an intriguing reversal of the sex-bias in lifespan was detailed between the settings: females live longer than males in nature but males outlive females in captivity. This study also confirmed an overall female advantage in body mass, despite sex-specific, seasonal body mass fluctuation in the wild. In the second study, no sex differences were found in the age trajectories of hand grip strength, an indicator of physical functioning, in either the captive or wild setting. Contrary to other species that invariably report stronger males than females, females were equally strong or stronger than males in the gray mouse lemur. To test the prediction that immune function might decline at old age, with more pronounced declines expected in males, in the third study I estimated the age trajectories of gastrointestinal parasite burdens (parasite prevalence and morphospecies richness quantified via fecal egg counts) as a proxy of overall health in the wild population. Contrary to these predictions, parasite burden declined with age similarly in both sexes, possibly due to acquired immunity and selective mortality of individuals with impaired resistance to parasites. However, males initially experienced a higher parasite burden. The fourth study was motivated by the finding that in other species, a high allostatic load follows from senescent deterioration in the negative feedback regulation of glucocorticoids, and has detrimental consequences for health and fitness. After validating an assay to quantify glucocorticoid levels from gray mouse lemur feces, I tested the prediction that aged animals would experience a high allostatic load. The prediction was met only in aged females in the dry season, perhaps indicating a reduced ability of the aged animals to cope with the energetic demands that coincide with the ecological dry season. In summary, I evidenced highly variable sex-, season-, and setting-specific patterns of senescence in the gray mouse lemur, with substantial differences in aging between the components of health measured. While senescent declines were observed in some parameters, an absence of senescence and even negative senescence were found in others. Body mass and parasite resistance were best preserved until old age, likely reflecting the importance of these indicators for survival and the associated strong, positive selective pressures for their maintenance. Contrary to the predictions of life history theory, wild males experienced generally a similar magnitude or less pronounced functional senescence relative to females. This implies that despite their early mortality, males do not experience earlier or faster senescence in the included components of health, perhaps due to strong selective pressures for a “robust” male phenotype required for improved male fitness. However, age-related changes in further components of functioning, including reproductive success, should be examined in both sexes to confirm these patterns. In conclusion, the results of this thesis do not support the fundamental predictions of an earlier onset or higher rate of senescence in the wild population that experiences high extrinsic mortality risk, or of an earlier senescence in the shorter-lived sex. The rapid, selective mortality of individuals in a declining condition and the associated positive selection for better self-maintenance may counteract the selective pressures that act to reduce self-maintenance beyond the prime reproductive age. The fitness-enhancing traits and the significance of selective mortality may differ across species and between the sexes. Further investigation into sex-specific, multi-trait senescence across taxa can shed further light on mechanisms of lifespan determination and the patterns of senescence observed across the animal kingdom, including
dc.contributor.coRefereeOstner, Julia Prof. Dr.
dc.subject.engsex differencesde
dc.subject.engphysical strengthde
dc.subject.engbody massde
dc.subject.engnatural populationde
dc.subject.enggray mouse lemurde
dc.subject.engMicrocebus murinusde
dc.affiliation.instituteBiologische Fakultät für Biologie und Psychologiede
dc.subject.gokfullBiologie (PPN619462639)de

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