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The Antarctic Ocean is one of the only places on earth where all biological processes happen between -2 and 2°C. At these temperatures, our models for life fall apart. Diffusion, protein folding, energy and metabolism are all processes that are poorly understood in the cold, where processes are slow and energy is scarce. The gap in our understanding of cold-adapted life comes partly from the lack of suitable equipment to properly observe these systems. Our team has recently developed a method to perform high resolution imaging of cold live samples, therefore shedding a new light to observe these systems in physiological conditions. The development of this new method offers perspectives for studying the rate of molecular, cellular and sub-cellular processes. Observing cells from Antarctic animals in vivo reveals some surprising dynamics, in particular when comparing the speed of organelle movement in the cold compared to temperate organelle speed. This opens avenues to investigate how the energy budget of cold-adapted cells is spent, and what survival strategies have evolved from such a constrained environment.
This new microscopy method could also be used to study the dynamics of similar systems when their environment is warming up, or for other applications in biotechnology, including but not limited to questions about phase separation, diffusion models and protein aggregation.


SEB Conference Prague 2024

Microscopes and Antarctic fish: How developing high-resolution microscopy for 0°C imaging sheds a new light on cold-adapted systems.

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SEB’s Annual Conference is celebrated for creating the perfect composition of research, new discoveries and collaborative connections. Be creative and innovative by exchanging ideas and knowledge with masters of biology from all over the world.

Climatic changes involved an important increase in the global mean surface temperature and frequency of heat waves, being a significant health risk reported in diverse big and medium-sized mammals. The analysis of energy expenditure components is key for understanding the processes of heat loss and thermoregulation. One of the highest heat expenditure activities is feeding; mammal metabolism can increase around 25-50% of the resting metabolic rate (RMR). It has been suggested that smaller animals could exhibit elevated fitness under warmer temperatures; however, this has not been tested on small wild mammals during the postprandial state. We addressed this issue in two non-endangered wild mouse species, the wood mouse (Apodemus sylvaticus) and the Algerian mouse (Mus spretus) kept in laboratory conditions. RMR and postprandial heat increment (HI) were measured by open flow respirometry at cool conditions (20°C) and within the thermoneutral zone (28°C). RMR was measured after overnight fasting of 16 -21 hours. Food was provided at 10% of the animal's body mass to evaluate the HI. We expected that mice would prioritize thermoregulation efficiency to food consumption. At warmer temperatures mice decrease their food intake to reduce HI, allowing efficient thermoregulation without compromising RMR. These adjustments could evidence possible changes in diet selection at higher temperatures related to the nutritional composition to reducing thermogenesis.

DOES THE TEMPERATURE INCREMENT AFFECT THE POST-PRANDIAL ENERGY METABOLIC RATE IN SMALL WILD MAMMALS?

The effect of temperature on biological functions can vary among individuals of the same species according to the environment they inhabit. In this sense, intraspecific variations in the energetic balance can provide insights on microevolutionary processes occurring at the population scale.
The aim of our work was to investigate intraspecific differences in fundamental energetic functions, namely energy acquisition via feeding, energy expenditure via standard metabolic rate, and energy allocation via growth in response to temperature, in a species living along a large latitudinal gradient. We exposed the common periwinkle, Littorina littorea, from 10 different locations in North America, to 12 temperatures (5 to 27 C) in a common garden experiment, and measured survival, feeding rate, growth, metabolic rate, and CTmax. Populations’ thermal performance curves were obtained and suggested that the thermal energy budget differs among different locations. Energy acquisition through feeding and energy allocation to growth differed only for locations at the species limits, which may be subjected to stronger selective pressure. Survival and CTmax were found to be lower at higher temperatures for snails from lower latitudes, this likely reflecting increased energetic needs for maintenance. However, the remarkable differences in the shape of metabolic rate may reflect local variations in energy expenditure strategies. Specifically, snails from different climates may use different strategies to adjust their energy budget to changing temperatures. Our study provides evidence of potential local and clinal adaptation of the investigated species to varying environmental conditions, helping to define its current (and likely future) range limits.


Variations in the energetic balance among populations of a marine gastropod living along a large latitudinal gradient.

Sediment runoff is a primary driver of coral reef degradation globally. Herbivorous fish (i.e., those that eat algae) are seen as a critical defense by managers worldwide to control the overgrowth of algae on corals. Yet, populations of these herbivores are rapidly declining on nearshore reefs impacted by sedimentation. Current evidence firmly establishes that fish gills undergo structural changes in response to increased levels of suspended sediment (SuS), suggesting a link between morphological alterations and potential respiratory impairment. Direct measurements of oxygen uptake in fish during SuS exposure would provide valuable insight into the physiological mechanism underpinning fish abundance. For this study, we 3D-printed novel respirometry chambers, explicitly designed with a cone-bottom shape, to allow sedimented water to enter underneath test fish and keep sediment suspended throughout respirometry experiments. Here, we present preliminary results on the oxygen uptake rate in the bioculturally important Pacific bullethead parrotfish, Chlorurus spilurus, measured not only post-exposure but also concurrently during exposure to SuS. We hypothesized that fish exposed to SuS would have a reduced metabolic scope and an extended recovery time to return to their standard metabolic rate—resulting in higher excess post-exercise oxygen consumption and signifying substantially reduced gill function. 



Metabolic responses to suspended sediment in a Hawaiian herbivorous reef fish

Vortical interactions permeate the natural world, from trout navigating streams to flying insects. These interactions serve to reduce the energy expenditure required for transportation while simultaneously enhancing thrust and lift. This study delves into the specific phenomenon known as wake capture, in which organisms harness the vortices shed from their own movements to extract or utilize energy. From jellyfish maneuvering through water to fruit flies navigating the air, wake recapture proves instrumental in minimizing energy expenditure. Through the analysis of three distinct case studies, we illuminate the significance of wake capture across various mediums: water, air, and at the interface. By comprehending the underlying principles and utilizing dimensionless numbers, a universal framework can be established to deepen our understanding of efficient locomotion across different environments.

Vortical interactions in nature

Warmer water temperatures and heat waves exacerbated by climate change are affecting the physiology and thermal tolerance of aquatic ectotherms, including fishes. Warming waters also alter infection dynamics with many species of parasites predicted to increase in prevalence and intensity as temperatures rise. Since parasites can alter host physiology, infection may have detrimental effects on host thermal tolerance. Ectotherms can increase their thermal tolerance through acclimation. Yet, the exposure time required for fishes to fully acclimate remains understudied. Furthermore, no studies have explored the interaction between parasite infection and acclimation time. We tested the effect of acclimation time on three pumpkinseed sunfish (Lepomis gibbosus) populations from lakes in Québec, Canada that differ in the prevalence and intensity of infection with helminth parasites. Pumpkinseeds were acclimated at either ambient (22°C) or +5°C (27°C) warm treatment for between 3h and 60 days and then tested in a critical thermal maximum (CTmax) protocol. CTmax in pumpkinseeds held at ambient temperature was highest in the uninfected lake. CTmax increased with acclimation time in all three lakes, but the speed of increase was slower in the two lakes with high parasite prevalence. However, these differences were not driven by individual infection intensity. Our findings indicate that prolonged acclimation time can influence the thermal tolerance of pumpkinseeds. Our study highlights the importance of considering different populations when studying a physiological trait and using adequate exposure time to fully acclimate the fishes.

Relationships among parasites and acclimation time on the upper thermal tolerance of three sunfish populations

Rapid global warming and increasingly severe heatwaves pose a serious threat to organisms in the Anthropocene. Aquatic ectotherms are especially at risk, as their body temperature generally matches that of the environment. Evolutionary adaptation is one of the few processes which might allow animal populations to better cope with these thermal challenges, yet it is rarely experimentally examined in vertebrates. Our group previously assessed the evolutionary potential for acute upper thermal tolerance by artificially selecting zebrafish on this trait, and found that evolution towards higher tolerance is possible but concerningly slow. We are currently conducting a new selection experiment using the same model species to study the evolution of thermal performance, which is distinct from acute thermal tolerance as it requires survival and resilience under chronic thermal stress. Based on growth performance in the juvenile life stage as the trait, we are selecting zebrafish to increase this performance at warm (34.5°C), control (28°C) or cold (20°C) temperatures. Starting with a genetically diverse ancestral population (6th captive generation offspring of wild-caught zebrafish, n>1000), we produced the F0 generation which was used to establish the respective warm-adapted, control, and cold-adapted lines. Each line consists of two replicates with ~300 fish/replicate, and we select the 33% with the highest growth rate to contribute to the next generation. Although this experiment is still ongoing, we present here the results for the F0 to F2 (n>5400) and place them in the context of key questions about the ability of animals to adapt to climate change.

Experimental evolution of thermal performance in zebrafish

Biodiversity is increasingly under threat due to climate events. Studies examining the impact of climate change on biodiversity often tend to focus on understanding species survival. However, for persistence of species, equal focus requires on reproduction, a process is more vulnerable to heat stress than survival. This vulnerability arises from the susceptibility of gametes and gonads at sublethal temperatures, with sensitivity levels varying across different life stages. Despite this knowledge, majority of existing studies tend to focus on the effects of heatwaves on juvenile or adult stages or/and neglecting the cumulative impact across life stages and potential recovery dynamics. To Address this critical gap, we used Drosophila melanogaster as a model to explore (i) how does heat stress at different life stages affect male reproduction? (ii) how does life stage-specific heatstress affect males’ ability to recover? (iii) What are the mechanisms underlying the reproductive consequences of heat stress? Our findings reveal that gametes and gonads are highly susceptible to heat stress. Cummulative and presistence effect of heat stress can severely damage male reproductive fitness. Such effects could speed up population declines due to loss of fertility, highlighting the need to include effects on reproduction and their recovery in studies of biodiversity loss.

Unravelling the impact of frequent heatwaves on insect reproduction

First, we used isolated hearts from three teleost species with very different values for maximum heart rate (fHMax: zebrafish, ~300 bpm; Atlantic salmon, ~120 bpm and lumpfish, ~80 bpm) to examine the response of intrinsic fH and atrioventricular delay (AVd) to acute changes in temperature. Heart rate increased linearly with temperature (Q10s of 1.91, 1.50 and 2.67 for zebrafish 16–28℃, salmon 8–20℃ and lumpfish 8–14℃, respectively), whereas AVd decreased (Q10 0.56–0.69). However, the absolute values for AVd showed considerable inter-specific variation. For example, the AVd at 16℃ for 28℃-acclimated zebrafish was ~2 and 3x shorter than that of 8℃-acclimated salmon and lumpfish, respectively. Further, we extrinsically paced their hearts (i.e., at 50, 100 and 150 bpm for zebrafish and 50, 70 and 90 bpm for lumpfish and salmon), and AVd decreased with temperature independent of pacing frequency (i.e., temperature had a direct effect on AV function). Next, we compared 8- vs. 15℃-acclimated salmon, and found that 8℃ fish: 1) exhibited cardiac resetting (i.e., had a higher fH from 12–20℃); 2) experienced 2:1 AV block ~1.7℃ earlier than warm-acclimated fish; and 3) had an ~20% shorter AVd at all test temperatures and pacing frequencies. Finally, we found that although conduction velocity (CV) was consistently ~100–300x faster across the ventricle and atrium than the AV funnel, it also exhibited a plastic thermal response. These data highlight the acclimation capacity of AVd and CV, and suggest that they are key contributors to cardiac thermal compensation and phenotypic plasticity.

Atrioventricular Delay and Cardiac Electrical Conduction Play Important Roles in Determining the Maximum Heart Rate of Fishes

During development, phenotype can be adaptively modulated by environmental conditions. However, as weather variability increases under climate change, the potential for maladaptive responses to environmental variations may increase. In the arid-adapted zebra finch, parents emit “heat-calls” when experiencing heat during incubation, which adaptively affects offspring growth in the heat, and adult heat tolerance. This suggests that heat-call exposure may adjust individual phenotype to hot conditions, potentially compromising individual sensitivity to cool weather conditions. To test this hypothesis, we manipulated individual prenatal acoustic and postnatal thermal experiences during development, and sought to assess subsequent chronic responses to thermal fluctuations at adulthood. We measured heterophil to lymphocyte (H/L) ratios in adults, when held in outdoor aviaries during two summers and two winters. We found that birds exposed to heat-calls as embryos, had consistently lower H/L ratios than controls at adulthood, irrespective of the season. Nonetheless, in all birds, the H/L ratio did vary with short-term weather fluctuations (2, 5 or 7 days), increasing at more extreme (low and high) air temperatures. In addition, the H/L ratio was higher in males than females. Overall, heat-call exposed individuals did not show a stronger chronic response in winter than control individuals, and instead appeared more resilient to thermal variability. Our findings therefore suggest that heat-call exposure did not compromise individual sensitivity to low temperatures at adulthood. Our study also reveals that prenatal sound can lead to long-term differences in individual physiology or quality/condition, which are consistent with previously-demonstrated reproductive fitness differences.

A prenatal acoustic signal of heat reduces a biomarker of chronic stress at adulthood across seasons in an arid-adapted bird

In a global change scenario, emerging infectious diseases are becoming more frequent and harder to prevent or control. In birds, malaria parasites are responsible for wildlife population declines of many species worldwide. Despite being exposed to the same risk, there is a clear inter-individual variation in the susceptibility to malaria. As hormone-mediated maternal effects may act as mechanisms of phenotypic plasticity facilitating the offspring's adaptation to new environments, here, we explored the dose-dependent response to maternal yolk hormones by experimentally injecting two different testosterone (T) doses into the egg yolks of wild great tits. High prenatal T levels could carry short-term benefits (i.e. accelerated metabolism and growth) but carry long-term costs including accelerated telomere shortening (i.e. a hallmark of ageing) and depressed immunity that could both increase susceptibility to malaria. Our preliminary results show no effects of T-treatment on body size or condition of nestlings, but chicks treated with the higher T-dose had higher breathing rates. Nestling survival to fledging was positively influenced by prenatal T (higher T-dose > control and lower T-dose), while we found no evidence of an effect on hatching success or post-fledging survival. The medium to long-term costs of prenatal T are currently investigated through post-natal telomere dynamics and malaria susceptibility measurements at the post-fledging stage, with the prediction that the short-term benefit of prenatal T should lead to shorter telomeres and accentuated malaria susceptibility. Future studies should carefully consider a range of concentrations, as the balance of costs and benefits of prenatal hormones may be dose-dependent.

Microscopes and Antarctic fish: How developing high-resolution microscopy for 0°C imaging sheds a new light on cold-adapted systems.

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DOES THE TEMPERATURE INCREMENT AFFECT THE POST-PRANDIAL ENERGY METABOLIC RATE IN SMALL WILD MAMMALS?

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