Journal of Experimental Biology最新文献

The 'thrifty female hypothesis' states that females preserve more of their energy reserves during winter than males because of the sex-specific time frame of energy allocation for reproduction. As males reactivate their reproductive axis before the mating period, while females mainly allocate energy during gestation and lactation, we hypothesized that males would have to use shorter torpor bouts and longer periods of normothermic activity to promote spermatogenesis during winter, a period of low food availability. Here, we applied an acute 2 week 80% caloric restriction in male and female grey mouse lemurs shortly before the mating period. We found evidence of thriftier phenotypes in wintering females, which performed deeper and longer torpor bouts than males and ultimately lost less body mass. Our results thus support the 'thrifty female hypothesis' in a seasonally breeding primate and reinforce the concept of a sex-biased trade-off in using torpor, which might ultimately benefit reproduction and survival.

Hummingbirds save energy by facultatively entering torpor, but the physiological mechanisms underlying this metabolic suppression are largely unknown. We compared whole-animal and pectoralis mitochondrial metabolism between torpid and normothermic ruby-throated hummingbirds (Archilochus colubris). When fasting, hummingbirds were exposed to 10°C ambient temperature at night and they entered torpor; average body temperature decreased by nearly 25°C (from ∼37 to ∼13°C) and whole-animal metabolic rate (V̇O2) decreased by 95% compared with normothermia, a much greater metabolic suppression compared with that of mammalian daily heterotherms. We then measured pectoralis mitochondrial oxidative phosphorylation (OXPHOS) fueled by either carbohydrate or fatty acid substrates at both 39°C and 10°C in torpid and normothermic hummingbirds. Aside from a 20% decrease in electron transport system complex I-supported respiration with pyruvate, the capacity for OXPHOS at a common in vivo temperature did not differ in isolated mitochondria between torpor and normothermia. Similarly, the activities of pectoralis pyruvate dehydrogenase and 3-hydroxyacyl-CoA dehydrogenase did not differ between the states. Unlike heterothermic mammals, hummingbirds do not suppress muscle mitochondrial metabolism in torpor by active, temperature-independent mechanisms. Other mechanisms that may underly this impressive whole-animal metabolic suppression include decreasing ATP demand or relying on rapid passive cooling facilitated by the very small body size of A. colubris.

Our current understanding of human gait is mostly based on studies using hard, level surfaces in a laboratory environment. However, humans navigate a wide range of different substrates every day, which incur varied demands on stability and efficiency. Several studies have shown that when walking on natural compliant substrates there is an increase in energy expenditure. However, these studies report variable changes to other aspects of gait such as muscle activity. Discrepancies between studies exist even within substrate types (e.g. sand), which suggests that relatively 'fine-scale' differences in substrate properties exert quantifiable influences on gait mechanics. In this study, we compared human walking mechanics on a range of sand substrates that vary in overall foot sinking depth. We demonstrated that variation in the overall sinking depth in sand was associated with statistically significant changes in joint angles and spatiotemporal variables in human walking but exerted relatively little influence on pendular energy recovery and muscle activations. Significant correlated changes between gait metrics were frequently recovered, suggesting a degree of coupled or mechanistic interaction in their variation within and across substrates. However, only walking speed (and its associated spatiotemporal variables) correlated frequently with absolute foot sinkage depth within individual sand substrates, but not across them. This suggests that a causative relationship between walking speed and foot sinkage depth within individual sand substates is not coupled with systematic changes in joint kinematics and muscle activity in the same way as is observed across sand substrates.

The Arctic is warming three times faster than the global average, imposing challenges to cold-adapted fish, such as Arctic char (Salvelinus alpinus). We evaluated stress and metabolic responses of Arctic char to different thermal acclimation scenarios to determine whether responses to thermal variation differed from those to stable exposures. Fish were exposed for 7 days to one of four treatments: (1) control (12°C); (2) mean (16°C), corresponding to the mean temperature of the diel thermal cycle; (3) constant high temperature (20°C); and (4) diel thermal cycling (12 to 20°C every 24 h). Exposure to 20°C causes increases plasma lactate and glucose, an imbalance in antioxidant systems, and oxidative stress in the liver. The 20°C treatment also elevated fractional rates of protein synthesis and caused oxidative stress in the heart. Stress responses were more pronounced in diel thermal cycling than in mean (16°C) fish, indicating that peak exposure temperatures or variation are physiologically important. Cortisol was highest in diel thermal cycling fish and oxidative stress was noted in the liver. Gill Na+/K+-ATPase activity was also significantly reduced in diel thermal cycling fish, suggesting gill remodeling in response to an osmoregulatory stress. Exposure to a constant 20°C was more challenging than a diel thermal cycle, demonstrating the importance of daily cooling to recovery. Arctic char inhabit a thermally variable environment and understanding how this impacts their physiology will be critical for informing conservation strategies in the context of a rapidly warming Arctic.

Mosquitoes cannot use metabolism to regulate their body temperature and therefore climate warming is altering their physiology. Mosquitoes also experience a physiological decline with aging, a phenomenon called senescence. Because both high temperature and aging are detrimental to mosquitoes, we hypothesized that high temperatures accelerate senescence. Here, we investigated how temperature and aging, independently and interactively, shape the antimicrobial immune response of the mosquito Anopheles gambiae. Using a zone-of-inhibition assay that measures the antimicrobial activity of hemolymph, we found that antimicrobial activity increases following infection. Moreover, in infected mosquitoes, antimicrobial activity weakens as the temperature rises to 32°C, and antimicrobial activity increases from 1 to 5 days of age and stabilizes with further aging. Importantly, in E. coli-infected mosquitoes, higher temperature causes an aging-dependent decline in antimicrobial activity. Altogether, this study demonstrates that higher temperature can accelerate immune senescence in infected mosquitoes, thereby interactively shaping their ability to fight an infection.

Energy is a common currency for any living organism, yet estimating energy expenditure in wild animals is challenging. Accelerometers are commonly used to estimate energy expenditure, via a dynamic body acceleration (DBA) or time-energy budget approach. The DBA approach estimates energy expenditure directly from acceleration but may lead to erroneous estimates during inactivity when acceleration is zero but energy expenditure is not. The time-energy budget approach uses accelerometers and other data streams to assign a behaviour to each time step, and then calculates energy expenditure based on activity-specific metabolic rates assigned to each behaviour. Here, we used GPS-accelerometry in breeding black-legged kittiwakes (Rissa tridactyla, n=80) to calculate DBA and time-energy budgets derived from simple biologging metrics (speed, wingbeat frequency, GPS position). We then compared these two approaches with estimates of energy expenditure from doubly labelled water (DLW). Energy expenditure estimated from DLW correlated with DBA, but the best model to estimate energy expenditure was based on time-energy budgets. Energetic costs of flapping flight were higher than all other kittiwake behaviours (5.54×basal metabolic rate, BMR). Energetic costs of gliding flight (0.80×BMR) were the lowest of all behaviours, and equivalent to the cost of resting at the colony. DEE for our birds estimated from our calibration coefficients was similar to DEE for our birds estimated with the model coefficient published using different methods. We conclude that once calibrated with DLW, GPS-accelerometry provides a simple method for measuring energy expenditure in wild kittiwakes based on time-energy budgets.

This study focuses on the nociceptive responses observed in the tobacco hornworm (Manduca sexta). While prior investigations have described the sensory neurons and muscle activation patterns associated with the 'strike' behavior, there remains a gap in our understanding of the alternative 'withdrawal' movement, wherein the animal bends its head and thorax away from the stimulus. Our results show that stimulus location determines which nocifensive behavior is elicited. Interestingly, stimulation of specific mid-body segments could result in either withdrawal or strike, indicating a decision process rather than a hard-wired circuit. The withdrawal behavior was characterized using high-speed videography and electromyography. The results show that withdrawal in Manduca is driven by contralateral ventral muscles, followed by an increase in ipsilateral muscle activation just before the bending stops. Dorsal muscles are co-activated throughout the movement. Although both withdrawal and strike behaviors involve sequential activation of lateral muscles, these behaviors involve different muscle groups. This discovery provides a novel model system to investigate the context-dependence and decision-making processes triggered by stressful or noxious stimuli.

Flying insects solve a daunting control problem of generating a patterned and precise motor program to stay airborne and generate agile maneuvers. In this motor program, each muscle encodes information about movement in precise spike timing down to the millisecond scale. Whereas individual muscles share information about movement, we do not know if they have separable effects on an animal's motion, or if muscles functionally interact such that the effects of any muscle's timing depend heavily on the state of the entire musculature. To answer these questions, we performed spike-resolution electromyography and electrical stimulation in the hawkmoth Manduca sexta during tethered flapping. We specifically explored how flight power muscles contribute to pitch control. Combining correlational study of visually-induced turns with causal manipulation of spike timing, we discovered likely coordination patterns for pitch turns, and investigated if these patterns can drive pitch control. We observed significant timing change of the main downstroke muscles, the dorsolongitudinal muscles (DLMs), associated with pitch turns. Causally inducing this timing change in the DLMs with electrical stimulation produced a consistent, mechanically relevant feature in pitch torque, establishing that power muscles in Manduca have a control role in pitch. Because changes were evoked in only the DLMs, however, these pitch torque features left large unexplained variation. We find this unexplained variation indicates significant functional overlap in pitch control such that precise timing of one power muscle does not produce a precise turn, demonstrating the importance of coordination across the entire motor program for flight.

In the hemipteran Rhodnius prolixus, successful post-prandial diuresis is accomplished through the synergistic actions of the peptidergic diuretic hormone RhoprCRF/DH and the biogenic amine 5-hydroxytryptamine (5-HT), and by an antidiuretic hormone RhoprCAPA-2 that terminates diuresis by inhibiting this synergy. Lateral neurosecretory cells (NSCs) in the mesothoracic ganglionic mass release RhoprCRF/DH, while midline NSCs release RhoprCAPA-2 during blood feeding. These NSCs co-express GPA2/GPB5, a conserved glycoprotein hormone involved in various physiological processes across bilaterians. This study investigates the influence of GPA2/GPB5 signaling on Malpighian tubule (MT) fluid secretion in R. prolixus. GPB5-like immunoreactivity in lateral and midline NSCs decreases following a blood meal, suggesting release and a role in diuresis. Downregulating the GPA2/GPB5 receptor LGR1 via RNA interference results in an increased basal fluid secretion rate in MTs, which is inhibited by the antidiuretic hormone RhoprCAPA-2. dsLGR1 treatment reduces the effects of RhoprCRF/DH and 5-HT on MT secretion and eliminates their synergism. RT-qPCR reveals that the transcript expression of the diuretic and antidiuretic hormone receptors are decreased in MTs of dsLGR1 injected insects, indicating that GPA2/GPB5 influences the expression of these other receptor transcripts. Downregulating LGR1 results in a smaller blood meal size and disrupts the normal time-course of diuresis. As LGR1 is the most abundantly expressed G protein-coupled receptor transcript in R. prolixus MTs, our results suggest that GPA2/GPB5 signaling has a critical role in regulating the timing and success of water retention in the unfed state, and in the complex processes associated with feeding and diuresis in R. prolixus.

Energy governs species' life histories and pace of living, requiring individuals to make trade-offs. However, measuring energetic parameters in the wild is challenging, often resulting in data collected from heterogeneous sources. This complicates comprehensive analysis and hampers transferability within and across case studies. We present a novel framework, combining information obtained from eco-physiology and biologging techniques, to estimate both energy expended and acquired on 48 Adélie penguins (Pygoscelis adeliae) during the chick-rearing stage. We employ the machine learning algorithm random forest (RF) to predict accelerometry-derived metrics for feeding behaviour using depth data (our proxy for energy acquisition). We also build a time-activity model calibrated with doubly labelled water data to estimate energy expenditure. Using depth-derived time spent diving and amount of vertical movement in the sub-surface phase, we accurately predict energy expenditure (R2=0.68, RMSE=344.67). Movement metrics derived from the RF algorithm deployed on depth data were able to accurately (accuracy=0.82) detect the same feeding behaviour predicted from accelerometry. The RF predicted accelerometry-estimated time spent feeding more accurately (R2=0.81) compared to historical proxies like number of undulations (R2=0.51) or dive bottom duration (R2=0.31). The proposed framework is accurate, reliable, and simple to implement on data from biologging technology widely-used on marine species. It enables coupling energy intake and expenditure, which is crucial to further assess individual trade-offs. Our work allows us to revisit historical data, to study how long-term environmental changes affect animals' energetics.