As ecosystems undergo global changes, there is increasing interest in understanding how organisms respond to changing environments. Recent evidence drawn from available vertebrate studies suggests that most of the phenotypic responses to climate change would be due to plasticity. We hypothesize that organisms that have evolved in unpredictable environments inform us about the mechanisms of phenotypic plasticity which provide an adaptive response to climate instability. As climate changes increase climatic hazards, these resilience mechanisms are expected to spread within species, populations and communities. We review studies that have demonstrated the importance of phenotypic plasticity in different life-history traits in overcoming climate uncertainty. We focus on organisms from unstable, recurrently energetically restrictive environments which possess a variety of morphological, physiological and/or behavioural adaptations to climate-driven selective pressures. First, we treat plastic morphological changes in response to fluctuating food availability. Adjustment of morphometric traits and/or organ size to energy supply would be essential in harsh environments. Second, we review the role of flexible energy-saving mechanisms, such as daily torpor, hibernation and energy storage, in overcoming climate-driven energetic shortages. Lastly, we address the role of plastic modulation of reproduction in fine-tuning the energy allocation to offspring production according to environmental conditions, with an emphasis on opportunistic breeding. Overall, we predict that species (or genotypes) possessing these efficient physiological mechanisms of resilience to unpredictable water and food fluctuations will be selectively advantaged in the face of increasing climatic instability.
There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.
SUMMARYAs ecosystems undergo changes worldwide, physiological flexibility is likely to be an important adaptive response to increased climate instability. Extreme weather fluctuations impose energetical constraints such as unpredictable food shortage. We tested how grey mouse lemurs (Microcebus murinus) could adjust their daily heterothermy and locomotor activity to these 'energetic accidents' with a food restriction experiment. The experimental design consisted of acute calorie restriction (2weeks, 80% restriction) in the middle of winter, after a fattening season with low (11weeks, 40% restriction) versus high (ad libitum) food availability. This design aimed at simulating the combined effects of the quality of the fattening season (acclimation effect) and a sudden, severe food shortage during the lean season. Hour of start and duration of torpor were the most flexible components of energy savings, increasing in response to the acute food shortage with facilitation by chronic restriction (acclimation effect). Modulations of locomotor activity did not support the hypothesis of energy savings, as total locomotor activity was not reduced. Nonetheless, acutely restricted individuals modified their temporal pattern of locomotor activity according to former food availability. We provide the first experimental evidence of different temporal levels of flexibility of energy-saving mechanisms in a heterotherm exposed to food shortage. The acclimation effect of past food scarcity suggests that heterothermic organisms are better able to respond to unpredicted food scarcity during the lean season. The flexible control of energy expenditure conferred by heterothermy may facilitate the plastic response of heterothermic species to more frequent climatic hazards. Supplementary material available online at
Summary1. Resource-limiting conditions impose a change in the energetic distribution between competing physiological processes. Over the past decade there has been increasing interest in trade-offs between the immune system and competing energy-consuming life-history traits. However, the trade-offs with energy saving mechanisms, such as heterothermy, have received limited attention. 2. The goal of this study is to determine how daily heterothermy expression could be adjusted to counterbalance the energetic requirements for the activation of the immune system depending on food availability (ad libitum vs. 40% calorie restriction) in a heterothermic primate, the Grey Mouse Lemur (Microcebus murinus). 3. On the day of the immune challenge, torpor was removed through the onset of fever, inducing a thermogenic cost. On the days following, food-restricted individuals returned to deep torpor (i.e. energy saving) whereas those fed ad libitum continued to skip torpor for at least three additional days. 4. The rapid return to an energy saving state in food restricted individuals raises new questions on the relationship between body temperature and immunocompetence. We suggest that (i) hyperthermia provides the first line of defence against pathogens, which is a trait common to all organisms, (ii) but that hypothermia may also protect the host by inhibiting pathogen proliferation.
Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.
Conditions experienced by individuals during prenatal development can have long-term effects on their phenotype. Maternally transmitted resources are important mediators of such prenatal effects, but the potential interactive effects among them in shaping offspring phenotype have never been studied. Maternally derived testosterone is known to stimulate growth, but these benefits may be counterbalanced by an increase in the production of reactive oxygen species (ROS). Maternally transmitted carotenoids might have the capacity to scavenge ROS and thereby buffer an increase in oxidative stress caused by prenatal exposure to high testosterone levels. Here, we experimentally tested for such interactive effects between maternal yolk testosterone and carotenoid in Japanese quail (Coturnix japonica). We found that hatching mass was reduced and reactive oxygen metabolites (ROMs) levels at the end of the period of maximal growth increased in chicks from eggs injected with either testosterone or carotenoid (only a tendency in chicks from testosterone-injected eggs). However, when both egg compounds were manipulated simultaneously, hatching mass and ROM levels were not affected, showing that both carotenoid and testosterone lose their detrimental effects when the ratio between the 2 compounds is balanced. Our study provides the first experimental evidence for interactive effects of 2 maternally derived egg compounds on offspring phenotype and suggests that developmental cues are tightly coadjusted within an egg. INTERACTIVE EFFECTS OF YOLK TESTOSTERONE AND CAROTENOID ON 10 PRE-NATAL GROWTH AND OFFSPRING PHYSIOLOGY IN A PRECOCIAL BIRD
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