France

For small, winter active endotherms living in cold ecosystems, thermal performance is critical for survival. Its unsurprising that populations of deer mice (Peromyscus maniculatus) adapted to high altitude, where ambient temperature is consistently lower than at sea level, have evolved an enhanced thermoregulatory capacity. As adults, these animals rely on an evolved, oxidative skeletal muscle phenotype to perform high rates of shivering thermogenesis. However, like most altricial mammals, the muscles of newborn deer mice are immature and unable to shiver. What happens when young animals face the same environmental challenges without the physiological tools as adults? In this talk I will discuss my recent work on the evolution of brown adipose tissue (BAT) and whole animal thermal performance in young Peromyscus mice. I have shown that during postnatal development, high altitude deer mice have evolved to suppress thermogenesis by impeding BAT function. I will discuss both the proximate and ultimate mechanisms we hypothesize are driving this phenomenon, including how BAT acts as an endocrine organ and may help program adult metabolic phenotype. These data will highlight how selection can act differently on the same physiological system depending on life stage.

SEB Conference 2022

Baby animals are not small adults! Proximate and ultimate mechanisms of brown adipose tissue evolution in the North American deer mouse

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2022 will find 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.
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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.

Diving as a lifestyle has evolved on multiple occasions when air-breathing terrestrial animals invaded the aquatic realm, and diving performance shapes the ecology and behaviour of all air-breathing aquatic taxa, from small insects to great whales. Using the largest dataset yet assembled, we show that maximum dive duration increases predictably with body mass in both ectotherms and endotherms. Compared to endotherms, ectotherms can remain submerged for longer, but the mass scaling relationship for dive duration is much steeper in endotherms than in ectotherms. These differences in diving allometry can be fully explained by inherent differences between the two groups in their metabolic rate and how metabolism scales with body mass and temperature. We therefore suggest that similar constraints on oxygen storage and usage have shaped the evolutionary ecology of diving in all air-breathing animals, irrespective of their evolutionary history and metabolic mode.

Universal metabolic constraints shape the evolutionary ecology of diving in animals

In birds, embryos use acoustic signals to synchronize hatching, learn calls or even solicit parental care. In zebra finches (Taeniopygia guttata), parents produce a peculiar “heat-call” during incubation at high ambient temperatures, which results in reduced nestling growth, in a temperature-dependent manner. Whilst being smaller may facilitate heat dissipation, we do not know whether being exposed to heat-calls prenatally affects thermoregulatory capacities and heat tolerance, and whether these effects persist into adulthood. Here, we tested the effects of experimentally delivered prenatal playback of heat-calls on thermoregulation at high temperatures at adulthood. We used a respirometry system to measure individuals’ metabolic rate and evaporative water loss at air temperatures (Ta) gradually increasing from 25°C to 44°C, while simultaneously monitoring their body temperature. Remarkably, prenatal exposure to heat-calls affected heat tolerance at adulthood, with individuals exposed to heat-calls as embryos more likely to reach the highest Ta in morning trials. This was despite higher metabolic rate and evaporative water loss in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At low Ta, however, heat-call exposed individuals had greater relative water economy, as predicted if heat-calls improve offspring thermoregulatory capacities. These results provide the first evidence that prenatal sound can have long-term effect on thermoregulation. Moreover, our findings point to a novel mechanism underlying developmental plasticity of thermal tolerance. 

Prenatal acoustic communication affects thermoregulation capacities in an arid-adapted bird.

Social behavior is an important part of the life of many animals with consequences for foraging and predator avoidance. In many species, individuals consistently vary in how social they are, which has consequences for group level dynamics. Recent work has found that individuals with a higher metabolic rate are less social, likely because they prioritize finding food over avoiding predators. In ectothermic animals like fish, temperature influences metabolic activity with higher temperatures leading to an increase in metabolic rate. As an individual fish moves through its environment, it is exposed to temporally and spatially different temperatures which could alter the individual motivation to engage in social behavior. Warming temperatures caused by climate change could also lead to reductions in social behavior and changes in overall group cohesion via effects on metabolic rate. However, the speed by which changes in metabolic rate affect expressed social behavior is not well understood. To test this, we acclimated common minnows (Phoxinus phoxinus) to three different temperatures (14, 17 and 20˚C) over 4 weeks.  We then measured maximum metabolic rate, standard metabolic rate and aerobic scope at acclimation temperature. In addition, we measured the routine metabolic rate, individual social behavior and group cohesiveness over a gradient of ramping temperatures (up to 23˚C). The results of this study will shed light into the effects of environmental change not only on an individual’s physiology and behavior but also on group behavior, which is essential to better predict the capacity of species to cope with climate change.

Effects of changing temperatures on social behavior via effects to metabolism in the common minnow (Phoxinus phoxinus)

The evolution of endothermy was instrumental to the diversification of birds and mammals, and enabled colonization of previously uninhabitable niches around the globe. However, in extreme environments such as high altitude, with extremely cold temperatures and limited O2 and food availability, the significant energetic demands of maintaining high body temperature (Tb) could offset the advantages of endothermy. We hypothesised that evolved reductions in Tb help overcome the metabolic challenges of cold hypoxia (CH) in deer mice native to high altitude. Deer mice with lowland or highland ancestry were held in warm normoxia (WN) or CH for 6 weeks, and then surgically instrumented with physiological telemeters. Mice in CH had significantly higher fH than mice in WN, underlain by reduced vagal tone and increased beta1-adrenergic tone on the heart, reflecting the metabolic challenges of CH. CH exposure led to marked reductions in Tb (~2˚C) in both lowlanders and highlanders. However, overlaid upon this plastic response to CH, highlanders had consistently lower Tb (~1˚C) than lowlanders. The combined effects of these plastic and evolved reductions in Tb were estimated to reduce metabolic demands by ~20%, based on theoretical expectations of Q10 effects and empirical measurements of the relationship between Tb and O2 consumption rate in these mice. Our results suggest that plastic and evolved reductions in Tb are important for overcoming the challenges at high altitudes, and provide a relatively rare example of evolved changes in Tb setpoint in a non-hibernating endotherm to cope with extreme environmental conditions.

Cool running: evolved reductions in body temperature and the metabolic costs of thermoregulation in deer mice native to high altitude

The oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis is the most prominent, albeit contentious, hypothesis aiming to explain the mechanisms setting thermal tolerance limits in ectotherms. At its core, the OCLTT hypothesizes that ectotherms lose performance at both low and high temperature thresholds due to metabolic oxygen demands exceeding supply capacities. Currently there is no consensus within the ecophysiology community regarding the universality of the OCLTT hypothesis, but there is a demand for an unbiased, systematic assessment of the existing literature. Therefore, we conducted a systematic review and several meta-analyses of studies testing core OCLTT predictions. Given the diverse range of experimental approaches used to test OCLTT predictions, we conducted quantitative syntheses for each relevant area. Additionally, to provide increased clarity on perceptions of the OCLTT hypothesis we surveyed the ecophysiology community involved in OCLTT research. The aim of this survey was to shed light on which variables are considered most relevant when testing OCLTT predictions, which experimental designs are considered valid tests of OCLTT predictions, and where further clarification around OCLTT predictions and assumptions are necessary. By combining quantitative tools to evaluate the OCLLT with a summary of the views and needs of the ecophysiology community, we aim to propel this area of research forward in positive manner. 

Using meta-analysis to resolve uncertainty around the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis

Anthropogenic increases in atmospheric CO2 levels are raising seawater temperatures, lowering seawater oxygen concentrations and pH (‘climate-related stressors’, CRS), among other changes. Under such change, some marine groups, such as stony corals, may have less ability to tolerate stress than others, potentially leading to population loss and thereby extinction. However, whether these vulnerabilities directly scale up to extinction risk, or tend to be somehow compensated e.g. by rapid range shifts, is unclear because few modern, global extinctions are unequivocally caused by CRS. We use meta-analysis to attempt a quantitative cross-scale evaluation of the role of CRS as extinction triggers. We do this by comparing individual responses to CRS in laboratory experiments and the range shift responses to global warming over recent decades, to extinction selectivity at ancient hyperthermal events and across the sum of metazoan evolutionary history, the Phanerozoic aeon. Clades and traits with strong negative responses to experimental CRS are most likely to go extinct at hyperthermal events, their genera also having the shortest geological durations. Among CRS, the synergistic combination of seawater warming and hypoxia has the most severe impact on marine organism performance. Response details suggest chiefly metabolic constraints in setting organism performance responses to CRS, which appear to scale up to extinction probabilities of past (and potentially future?) hyperthermal events. Ecological experiments are the only way to test underlying physiological mechanisms. Meanwhile, the fossil record documents myriad extinctions, often with strong selectivity patterns, that amount to mass proportions under hyperthermal conditions. Uniting the strengths of the two approaches may enrich our abilities to predict the future.

A dangerous synergy of warming and hypoxia: the past and present for the future

Phenotypic plasticity can increase resilience of animals to environmental change, and can therefore be important in naturally variable environments and under anthropogenic climate change. Phenotypic plasticity presents at three time scales, within-individual acclimation, developmental plasticity, and transgenerational effects. These different forms of plasticity can adjust phenotypes to at least partially buffer the organism from potentially harmful environmental conditions. Plasticity can thereby be important for population persistence and species survival. Conservation is commonly applied in a species-specific ecological context. However, it may be that populations within species have different capacities for plasticity, which may render the species as a whole more resilient to change via the portfolio effect. We tested this hypothesis by implementing novel meta-analytic approaches to quantify plastic capacities across populations of ectothermic species. We determined whether moderators including ecosystem (aquatic and terrestrial), plastic mechanisms (acclimation, developmental and transgenerational) and environmental variables (temperature and salinity) impact variability in plasticity between populations. The outcome of this study are important for conservation and in an evolutionary context to understand the complexity of transient responses to environmental change within species.

Are there differences in plasticity between populations within species?

Ectothermic animals represent most of the animal diversity on the planet and yet, are the most challenged by rising temperatures. As such, understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Neglecting how early environmental experiences shape thermal tolerance (i.e., developmental plasticity) may be an important oversight given that early life experiences have major and often persistent effects on phenotypes. To quantify the acute and persistent influence of early thermal environments on thermal tolerance, we systematically reviewed 6000 studies and meta-analysed data from 150 studies. In this talk, I will address the following questions: How much do early thermal environments impact heat tolerance, and is that enough to compensate for rising temperatures? Are embryos more plastic than juveniles? Do early thermal environments have persistent influence on heat tolerance? What is the current state of knowledge and what are pressing future directions in the field?

Developmental plasticity in thermal tolerance: ontogenetic variation, persistence, and future directions

Many ectotherms have shown a reduction in maximum body size in the past decades in parallel with climate warming. The gill-oxygen limitation (GOL) hypothesis is a prominent concept regarding the physiological mechanisms underlying the observed trends, implicating oxygen uptake limitations in driving the decline in fish body size with warming. Investigations of GOL have largely been theoretical and therefore the hypothesis’ merit has been questioned. We performed a literature review of the allometry of gill surface area (GSA) and metabolic rate. Furthermore, we reared barramundi under optimal, warm and cold conditions and measured metabolic rate and GSA at various time points. In our analyses, we introduced a new parameter, the ratio S, which provides a measure of GSA in relation to the metabolic requirements for maintenance (SSMR) and maximum activity (SAMR). Contrasting with the GOL hypothesis, we show that scaling exponents for S are consistently close to zero, with only a few exceptions where S either increased or decreased. We further demonstrate that S only decreases with body size when fish are acclimated to cooler-than-optimal temperatures, and not, as predicted by GOL, when temperatures rise. This suggests that GSA is sufficient to meet fish oxygen requirements even when temperatures increase, and that growth is not universally restricted by oxygen supply limitations at the gills. We identify the need to investigate alternative hypotheses to help explain the observed declines in maximum fish body sizes with climate warming, to facilitate accurate forecasts of fish populations and fisheries in the face of climate change.

Investigating the gill-oxygen limitation hypothesis in fishes: intraspecific scaling relationships of metabolic rate and gill surface area

Life history strategies are incredibly diverse across taxa, yet traits covary predictably along a fast-slow continuum such that species exhibit a distinct pace-of-life. Theory puts acquisition-allocation trade-offs at the core of life history evolution; however, reproductive investment in species with different reproductive modes can modify acquisition-allocation trade-offs which ultimately alters their life history. While metabolic rate has been touted as a key explanation for pace-of-life across diverse taxa some consider trade-offs between current and future reproduction as being more influential. Other evidence points to environmental variation playing an overarching role. No comparative study has attempted to disentangle these competing explanations. Here, we integrate physiological, reproductive and ecological data across more than 500 terrestrial ectotherms (snakes, lizards and the tuatara) where viviparity has arisen independently over 100 times throughout their evolutionary history. Applying a single multivariate phylogenetic framework, we test how metabolic rate, the environment and reproductive investment contribute in explaining the (co)variation in age at maturity and life span. We also determine if the importance of these factors vary according to reproductive mode (oviparous and viviparous taxa). Overall, while metabolic rate had a negative impact on age at maturity and lifespan, there was high heterogeneity among taxa in its relative role. Age at maturity and lifespan were strongly influenced by the environment, possibly through its effect on mediating activity patterns. Relative reproductive investment was also moderately important in predicting variation in age at maturity but not lifespan, particularly in oviparous species. Our results exemplify the complex nature of life history evolution. We highlight environmental drivers and its effect on patterns of growth, resource availability and mortality as likely sources of life history variation.

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