Abstract
In seasonal environments, males and females usually maintain high metabolic activity during the whole summer season, exhausting their energy reserves. In the global warming context, unpredictability of food availability during summer could dramatically challenge the energy budget of individuals. Therefore, one can predict that resilience to environmental stress would be dramatically endangered during summer. Here, we hypothesized that females could have greater capacity to survive harsh conditions than males, considering the temporal shift in their respective reproductive energy investment, which can challenge them differently, as well as enhanced flexibility in females' physiological regulation. We tackled this question on the gray mouse lemur (Microcebus murinus), focusing on the late summer period, after the reproductive effort. We monitored six males and six females before and after a 2-weeks 60% caloric restriction (CR), measuring different physiological and cellular parameters in an integrative and comparative multiscale approach. Before CR, females were heavier than males and mostly characterized by high levels of energy expenditure, a more energetic mitochondrial profile and a downregulation of blood antioxidants. We observed a similar energy balance between sexes due to CR, with a decrease in metabolic activity over time only in males. Oxidative damage to DNA was also reduced by different pathways between sexes, which may reflect variability in their physiological status and life-history traits at the end of summer. Finally, females' mitochondria seemed to exhibit greater flexibility and greater metabolic potential than males in response to CR. Our results showed strong differences between males and females in response to food shortage during late summer, underlining the necessity to consider sex as a factor for population dynamics in climate change models.
Highlights
In highly seasonal environments, reproduction has evolved to be restrained to the most energetically favorable period to optimize young growth (Fournier et al, 1999), which is a fragile and high-stake phase though crucial to ensure population renewal (Wells, 2000)
Females began the experiment with a higher body mass (BM) than males (99.7 ± 3.8 g vs. 90.0 ± 6.6 g, p < 0.05; Figure 1B), caloric restriction (CR) induced similar BM loss in both females and males (−16.7 ± 4.3% of the initial BM for females and −14.2 ± 4.3% of the initial BM for males, p > 0.05, Table 1) though taking into account the significant effect of the initial BM on BM loss (p < 0.01)
We found evidence of sex-specific regulation of metabolic activity in mouse lemurs submitted to CR at the end of summer, which could compel with their own programmed physiological and behavioral agenda
Summary
Reproduction has evolved to be restrained to the most energetically favorable period to optimize young growth (Fournier et al, 1999), which is a fragile and high-stake phase though crucial to ensure population renewal (Wells, 2000). With more frequent climatic disturbances related to global warming, there is no longer certainty that summer will support such energetic demands (Canale and Henry, 2010). This season might become a risky period, where animals, exhausted after their reproductive effort, would be more vulnerable to environmental change and become unable to compensate unexpected altered food availability. Seasonality could have contributed to establish a phenological shift in the energetic investment for reproduction between males and females. In a context of more frequent unpredictable climatic disturbances, we ask the question of a sex-imbalance in the trade-off between reproduction and survival and consider the hypothesis of a greater exhaustion in males than in females at the end of summer
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