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The body size of an animal is a key driver of ecological traits such as fecundity, mortality and growth. Ectotherms mature at smaller body sizes in warmer conditions and under low oxygen availability (hypoxia). Whether these size reductions are driven by a decrease in cell size or cell number (which together determine body size) and how such cellular responses may help ectotherms cope with thermal challenges and hypoxia is poorly understood. The theory of optimal cell size postulates that cell size impacts metabolic costs and the capacity of cells to take up oxygen via differences in surface-to-volume ratio. In this way, cell size has consequences for growth rate and body size. Here, using inbred lines of fruit flies Drosophila melanogaster, which exhibits differences in cell size, we investigate how body size reductions due to warming or hypoxia are modulated by and result from differences in cell size. Temperature-size responses were stronger under hypoxia and in lines of flies exhibiting large cell sizes, supporting the idea that larger cells constrain organismal growth by their inherently lower capacity for oxygen uptake. Reductions in body size were driven by reductions in cell size, whereas cell number increased to compensate partially. Thus, a cellular perspective offers a complete understanding of changes in body size in response to temperature and oxygen.

SEB Conference 2022

The role of cell size in shaping responses to oxygen and temperature in fruit flies

technical paper

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2022 found over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France.

Decades of research on the physiology of amphibians and non-avian reptiles suggest that both subcellular and organ system mechanisms are important in determining thermal tolerance limits, with hierarchical effects. We propose an integrated framework, which we call Hierarchical Mechanisms of Thermal Limitation (HMTL), which combines ideas from the thermal performance curve paradigm, oxygen limitation hypothesis, and marginal stability hypothesis. This unified framework can explain how processes interact to limit performance and set tolerance limits at high temperatures. We tested this framework in experiments with the upslope-colonizing lizard, Podarcis muralis. In line with the predictions of the HMTL hypothesis, the critical thermal maximum and anaerobically-fueled sprint speed are unaffected by acute mild hypoxia, while both the maximum aerobic scope and the optimal temperature for aerobic scope are reduced. We then developed a mathematical framework, which we call Temperature-Oxygen Performance Surfaces (TOPS), that provides sensitivity parameters which quantify how performance traits vary in response to oxygen availability or capacity. This novel framework is transferable across traits and levels of organization to allow predictions for how ectotherms will respond to novel combinations of temperature and other abiotic factors, an essential tool in a time of rapidly changing environmental conditions.

Interactive effects of temperature and oxygen availability on performance and thermal limits in the lizard Podarcis muralis

Predicting the responses of organisms to environmental change requires understanding the correlation between behavioral and physiological traits so as to avoid overheating without compromising performance. The concept of coadaptation, i.e., the correlation between thermoregulatory behavior and thermal physiology, is a foundational principle in evolutionary physiology. Yet, phylogenetic comparative analyses provide mixed support for coadaptation or evolutionary trade-offs. Few analyses of coadaptation between behavior and physiology include both a phylogenetic and an environmental context. Evidence for trade-offs maybe scarce, because the covariation between traits may be constrained by responses to local environmental conditions. Here we quantify how constraints in core thermal and behavioral trait may modulate patterns of coadaptation. We estimated thermoregulatory behavior and thermal physiology for 12 species of Phrynosomatid lizards inhabiting the Sonoran desert. We found low phylogenetic signal in traits associated with behavioral thermoregulation. Yes, behavioral traits have rates of evolution 3x higher than physiological traits associated with locomotor performance and temperature tolerance. When we modeled state-dependent shifts in thermal physiology as a function of thermoregulatory behavior, we found that thermoregulatory behavior did not influence the rate of evolution in thermal physiology. As environmental change may favor new combinations of behavioral and physiological traits, evolutionary mismatches between these traits can become exaggerated and result in novel phenotypic trajectories and result in a breakdown of thermal coadaptation. Our study revealed partial coadaptation and limited evidence for tradeoffs between thermoregulation and thermal physiology, which could be the default evolutionary pattern in the evolution of these traits, which has major implications for studying thermal coadaptation as environments change worldwide.

Evolutionary trade-offs between thermoregulatory behavior and thermal physiology in an assemblage of Sonoran desert lizards

Variability in the environment defines the structure and dynamics of all living systems, from cells to organisms to ecosystems. Species have evolved traits and strategies that allow them to detect, exploit and predict the changing environment. These traits allow organisms to maintain steady internal conditions required for physiological functioning through feedback mechanisms that allow internal conditions to remain at or near a set point despite a fluctuating environment. In addition to feedback, many organisms have evolved feedforward processes, which allow them to adjust in anticipation of an expected future state of the environment. Here I provide a framework describing how feedback and feedforward mechanisms operating within organisms can generate effects across scales of biological organization, and how they allow living systems to persist in fluctuating environments. I demonstrate how daily, seasonal and multi-year cycles provide cues that organisms use to anticipate changes in physiologically-relevant environmental conditions. Using feedforward mechanisms, organisms can exploit correlations in environmental variables to prepare for anticipated future changes. Strategies to obtain, store and act on information about the conditional nature of future events are advantageous and are evidenced in widespread phenotypes such as circadian clocks, social behaviour, diapause, and migrations. Finally, I show how humans are altering the ways in which the environment fluctuates, causing correlations between environmental variables to become decoupled, decreasing the reliability of cues. Human-induced environmental change is also altering sensory environments and the ability of organisms to detect cues. Recognizing that living systems combine feedback and feedforward processes is essential to understanding their responses to current and future regimes of environmental fluctuations.



Life in fluctuating environments

The capacity of ectotherms to adjust their heat limits through evolution or acclimation seems relatively modest and highly variable, and we lack satisfying explanations for both findings given a limited understanding of what ultimately determines an organism’s heat limit. Here, we propose that the amount of heating an ectotherm can tolerate should scale with temperature’s influence on biological rates and therefore the effective duration of biological processes. We tested this hypothesis by analyzing heating tolerances of diverse ectothermic taxa acclimated to different temperatures, and rescaling the duration of heating events to account for the non-linear influence of temperature on biological rates and thus, on the way organisms experience time. This rescaling reveals that the rate-corrected heating tolerance of an organism is in fact remarkably constant across any acclimation temperature, enabling high-precision estimates of how their heat limits will vary under different thermal regimes. We also find that faster heating rates consistently reduce rate-corrected heating tolerances, which helps further explain why heat limits seem so variable. Existing paradigms are that heating tolerances and heat limits are constrained by evolutionary conservatism or index failure of systems such as membrane function; our data provide a different perspective and show that an organism’s heat limit emerges from expenditure of rate-corrected heating tolerance, which is an approximately-fixed property of a species.

Heating tolerance of an ectotherm does not vary when temperature’s influence on biological rates is accounted for

Temperature affects many aspects of spruce budworm (SBW) fitness, including survival and development; therefore, there we hypothesized there would be strong selection for local adaptation of cold tolerance and the capacity to increase it We know that regional populations are capable of plastic responses to stressful low temperature conditions, however we have limited knowledge of the biochemical mechanisms underlying these responses. Cold tolerance is closely tied to glycerol production as glycerol is the most prevalent cryoprotectant in SBW.  Yet glycerol synthesis must come at the cost of glycogen reserves, which also form the only overwintering energy store.  We hypothesized that local adaptation for increased glycerol synthesis has occurred in SBW, and predicted that fluctuating temperatures (which increase glycerol synthesis) would induce increased enzyme activity in the pathway responsible for glycerol synthesis, and that more northerly populations would have higher enzyme activity than more southerly populations.  We developed enzyme activity assays for three key enzymes in the SBW glycerol synthesis pathway: glucose-6-phosphate dehydrogenase (G6PDH), phosphoglucoisomerase (PGI) and phosphofructokinase (PFK).  We then assayed the activity of these enzymes  in SBW from five populations (NWT, Alberta, New Brunswick, Quebec, and IPQL) reared in common garden conditions and then following fluctuating cold exposure to assess enzymatic reaction rate (Vmax) and enzyme substrate affinity (Km) to characterize changes in potential glycerol synthesis. Here we show that Km was not changed by either population origin or experimental conditions, but Vmax is frequently affected by both, illuminating a mechanism of adaptation to extreme temperatures.

Local adaptation in the plasticity of cold tolerance in the eastern spruce budworm

Abstract: Forecasting the long-time consequences of global warming requires knowledge not just on thermal mortality but also how heat stress interacts with other environmental stressors1,2. Here we describe an analytical framework that combines laboratory measurements and high 
resolution field temperature records to      forecast      mortality 
risks over the next century. As a proof of concept, we study amphipods Dikerogammarus villosus and Echinogammarus trichiatus from river Waal, Netherlands, acclimated to different temperatures and oxygen levels. We predicted daily and annual heat mortality in the river under different 
oxygen levels for current temperatures      and for 1 ºC and 2 ºC 
warming     . Given the p     rojected increases in      summer 
temperatures,      annual mortality is forecasted to increase 
substantially during the next decades, varying with acclimation status 
and water oxygenation. Both      acclimation to elevated water 
temperatures and adequate oxygenation are      crucial for persistence 
under current temperatures. However, even in the best case scenario,     
  mortality in D. villosus is expected to approach 100 % by 2100, while E. trichiatus appears to be less vulnerable. Overall, this framework generates forecasts in unprecedented detail on short- and long-term temporal impacts of rising temperatures in ecological communities, and also the contribution of other environmental stressors.

Long-term forecast of thermal mortality with climate warming in amphipods from a temperate river

Interactions between plants and herbivores are essential for land ecosystems, and their diversity is driven by an evolutionary arms race between plant defences and insect counteradaptations. Plants protect themselves against herbivory by chemical and physical defences, while many insects have evolved mechanisms to overcome these. Compared to chemical plant defences, little is still known about the role of physical defences and insect counteradaptations. We investigated the role of hooked trichomes in Passiflora adenopoda as a physical defence against herbivores and how certain Heliconius caterpillars can cope with these trichomes. Behavioural assays and video analysis showed that hooked trichomes of P. adenopoda arrested the movement of "generalist" H. melpomene caterpillars, and killed them by piercing their cuticle. Moreover, if H. melpomene caterpillars managed to ingest trichome-bearing leaves without external injuries, they still always died. As the caterpillars developed normally when fed with leaves where trichomes had been "shaved", this effect must be based on internal mechanical damage. We found that ingested hooked trichomes penetrated the gut peritrophic matrix in H. melpomene caterpillars. By contrast, "specialist" Heliconius charithonia caterpillars could easily crawl over the leaves by pulling their prolegs away from the trichomes. They also successfully fed on trichome-bearing leaves, likely due to modifications in their gut peritrophic matrix. Light and scanning electron microscopy of the caterpillars' cuticle and the gut peritrophic matrix revealed characteristic differences between both Heliconius species. Our study helps to understand an important but as yet little-explored aspect of the evolutionary arms-race between Passiflora and Heliconius

Game of thorns: How hooked trichomes protect plants from herbivory and how specialised

Atlantic killifish are found in estuarine habitats along the Atlantic coast of North America. In these habitats, fish are exposed to thermal variation at multiple scales - at timescales from days to seasons, and across latitudes, such that the northern subspecies is locally adapted to cold temperatures, and the southern subspecies to warm temperatures. The northern and southern subspecies differ substantially in mitochondrial properties, with mitochondria from northern fish having greater respiratory capacity, which likely helps to support their greater whole-organism aerobic metabolic rates. However, this pattern is only observed in mitochondria from the liver, and not in mitochondria from the heart or the brain, emphasizing the importance of examining mitochondrial properties across tissues. We also find differences in mitochondrial oxygen affinity between species (assayed in liver mitochondria), with mitochondria from southern fish having greater oxygen affinity, consistent with their superior whole organism hypoxia tolerance. In addition to the putatively adaptive variation, both subspecies demonstrate substantial plasticity in mitochondrial properties. Acclimation to high temperature results in a strong suppression of mitochondrial capacity in both subspecies, mediated upstream of cytochrome c oxidase, which may help to compensate for the effects of acute exposure to high temperature on reaction rates.  In contrast, acclimation to low temperatures causes relatively modest increases in mitochondrial capacity, but in the northern subspecies only, it also causes substantial increases in mitochondrial density. These data demonstrate the many ways that mitochondrial properties are shaped by both plasticity and adaptation in this small fish.

Plasticity and adaptation in mitochondrial function in killifish

Mitochondrial function [e.g., respiration, respiratory coupling ratio (RCR) and reactive oxygen species (ROS) production] is negatively impacted by high temperatures, and may limit fish cardiac performance and upper thermal tolerance. Nevertheless, direct evidence of this is lacking, and testing at different levels of organization will be critical to establishing whether this construct has validity. We acclimated salmon to 10 and 20°C for &gt;2 weeks and then: used strips from half of the ventricle to simultaneously measure muscle work and O2 consumption (and thus efficiency) at 20 and 26oC; and the other half to obtain myocardial homogenates and isolated mitochondria so that mitochondrial functional parameters could be measured at the same temperatures. State 4 respiration for isolated mitochondria and State 2 respiration for homogenates, and absolute ROS production during these states, were positively correlated with resting muscle O2 consumption in fish acclimated to both temperatures. In contrast, we were unable to consistently identify relationships between mitochondrial parameters and O2 consumption/efficiency while the muscle was working. For example, the P:O ratio (Complex I) and RCR (Complex I+II) for these preparations were not related to the absolute efficiency of shortening work. Further, while total CI+CII ROS production was negatively correlated with the efficiency of shortening work in 20oC acclimated salmon, this relationship was not evident for 10oC acclimated fish. These results: are consistent with previous data showing that warm acclimation improves cardiac mitochondrial function at high temperatures; but only provide a tenuous link between heart and mitochondrial performance in salmon under such conditions.

Are Cardiac Muscle Performance and Mitochondrial Function Related in Atlantic Salmon (Salmo salar) at High Temperatures?

There is a wealth of evidence for the impact that early-life conditions, e.g., differences in growth rate, have on individuals’ later-life phenotype and performance. Mitochondria are believed to be a key player in this, as they not only fuel the cellular processes but are also involved in health and age-related disorders. Birds have surprisingly slow ageing rates and long lifespans for their body size and physiology. Recent work with avian models has highlighted the utility of determining mitochondrial function in their nucleated red blood cells (RBCs), which enables longitudinal sampling of mitochondria within individuals as they age. Here, we employ this new perspective to test, using zebra finches (Taeniopygia guttata), whether modifying an individual’s postnatal growth trajectory, using an ecologically-relevant scenario, results in consistent changes in adulthood mitochondrial functioning and if these relate to individual’s survival. Our results demonstrate that within individual age-related changes in mitochondrial function can be detected using RCBs in birds and they are evident by middle age. However, despite that some of the mitochondrial traits show individual consistency, we found no link between adult RBCs mitochondrial function and the pace of early growth or mid-term survival. Further research across the life course will help to interpret the implications of the observed changes for individual performance and its sensitivity to environmental changes.

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