The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.
Current discussions in evolutionary ecology and conservation genetics focus on the relative importance of using selective neutral markers or markers of coding genes to identify adaptive and evolutionary relevant processes. Genetic diversity might be particularly important in immune genes (e.g., in genes of the major histocompatibility complex, MHC), which are influencing pathogen and parasite resistance. We investigated the effects of neutral versus adaptive genetic variation in parasite resistance in a natural population of fat-tailed dwarf lemurs (Cheirogaleus medius). No association between neutral overall individual genetic diversity and parasite load could be detected. In 149 individuals, we identified 50 MHC class II alleles of the functionally important duplicated DRB locus. The investigation of the functional importance of immune gene (MHC) diversity and parasite selection in natural populations is often problematic due to extensive polymorphism in the MHC genes and restrictions in available sample sizes. Here, for the first time we applied an approach that has been developed in human medical studies. Eleven MHC class II supertypes were identified based on shared antigen-binding similarities. The number of individual MHC supertypes had no influence on the nematode burden. However, we found evidence for a specific MHC supertype (supertype 1) that was linked to infected individuals, a higher number of different nematode infections and high intensity of infection per individual. Moreover, one rare MHC supertype (supertype 7) was revealed to be advantageous with respect to parasite burden. Thus, our results add evidence to the small body of studies that show significant associations between specific MHC constitutions and naturally occurring parasites in the complexity of natural populations.
The Malagasy primate Cheirogaleus medius hibernates in tree holes for 7 months, although ambient temperatures during hibernation rise above 30 degrees C in their natural environment. In a field study we show that during hibernation the body temperature of most lemurs fluctuates between about 10 degrees C and 30 degrees C, closely tracking the diurnal fluctuations of ambient temperature passively. These lemurs do not interrupt hibernation by spontaneous arousals, previously thought to be obligatory for all mammalian hibernators. However, some lemurs hibernate in large trees, which provide better thermal insulation. Their body temperature fluctuates only little around 25 degrees C, but they show regular arousals, as known from temperate and arctic hibernators. The results from this study demonstrate that maximum body temperature is a key factor necessitating the occurrence of arousals. Furthermore, we show that hibernation is not necessarily coupled to low body temperature and, therefore, low body temperature should no longer be included in the definition of hibernation.
In this field study, the energetic properties of tropical hibernation were investigated by measuring oxygen consumption and body temperature of the Malagasy primate Cheirogaleus medius in their natural hibernacula. These lemurs use tree holes with extremely varying insulation capacities as hibernacula. In poorly insulated tree holes, tree hole temperature and body temperature fluctuated strongly each day (between 12.8 and 34.4 degrees C). The metabolic rate under these conditions also showed large daily fluctuations between about 29.0 ml O(2)/h and 97.9 ml O(2)/h in parallel with changes in body temperature. In well insulated tree holes in very large trees on the other hand, tree hole temperature and body temperature remained relatively constant at about 25 degrees C. Lemurs hibernating in these tree holes showed a more constant metabolic rate at an intermediate level, but hibernation was interrupted by repeated arousals with peak metabolic rates up to 350 ml O(2)/h. The occurrence of these spontaneous arousals proved that the ability for thermoregulation persists during hibernation. Arousals were energetically costly, but much less so than in temperate and arctic hibernators. Despite the decisive influence of tree hole properties on the pattern of body temperature and metabolic rate during hibernation, the choice of the hibernaculum does not seem to be of energetic importance. The overall energetic savings by tropical hibernation amounted to about 70% as compared to the active season (31.5 vs. 114.3 kJ/d). Therefore, tropical hibernation in C. medius is an effective, well-regulated adaptive response to survive unfavourable seasons.
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