France

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.

SEB Annual Conference 2022

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

Discover the art of creating extraordinary science at SEB’s Annual Conference at Le Corum Conference Center     in Montpellier, France from 5 to  8 July 2022.

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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 - Montpellier, France

technical paper

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.

What predicts pace-of-life? Distinguishing among multiple hypotheses in terrestrial ectotherms

Human migration into urban areas has increased urbanization worldwide. As natural areas become urbanized, animals are forced to migrate, adapt, or perish in response to drastic habitat changes. Studies have documented how animals respond to the changes in biotic and abiotic factors associated with urbanization. Mostly, these studies document changes in phenotypic traits—morphology, physiology, and/or behaviors. With so many studies now available, meta-analyses offer insights into whether general trends in phenotypic responses among animals occur with urbanization. My lab has used phylogenetic meta-analyses to understand whether certain animal groups exhibit consistent phenotypic responses to urbanization, and to determine if the phenotypes of animals are consistently different across cities within studies. We have found that lizards—an animal group which has many urban-dwelling species—generally respond to urbanization through changes in body size. Urban lizards are larger than their non-urban counterparts. However, among all animal groups, the effects of urbanization depend on how many cities are included in a study, and the geographic distance between those cities. Phenotypic differences between urban populations of the same species increase as the more cities are investigated and as the farther away cities are from each other. Thus, separate urban populations of the same species can diverge phenotypically. Overall, it remains difficult to generalize the effects of urbanization on animal phenotypes with the current state of the literature. As more research emerges, meta-analyses will help us recognize if and how animals respond to human-induced habitat changes.

Using meta-analyses to understand phenotypic responses to urbanization in animals

Using examples of insect-plant interactions, I will show how biomechanical research can provide important insights into ecological and evolutionary questions. Insect-plant interactions must always be studied at least partially in the field, as essential aspects of their biology can be overlooked in the laboratory. Biomechanical factors play an important role in many insect-plant interactions such as pollination, herbivory and plant carnivory. Similar to the effects of plant chemical compounds or optical cues, plants can use mechanical ways to manipulate insect behaviour. For example, rockroses can mechanically detect visiting insects and guide pollinators to as yet unpollinated flowers, hollyhocks deploy slippery petals to guide insects to the fertile flower parts, and some pitcher plants have developed climbing barriers that prevent insects from walking around the pitcher to direct them to the slippery trapping surfaces. Again analogous to chemical factors in interactions, biomechanical factors can lead to adaptations and counter-adaptations, with far-reaching ecological and evolutionary consequences. The complexity of biological effects resulting from biomechanical factors is illustrated by Macaranga ant-plant mutualisms, where 'wax barriers' and 'wax-running' ants have triggered a whole range of secondary secondary ant and plant adaptive traits, including the presentation of food, epidermis longevity, the presence of preformed entrance holes, and ant colony density and aggressiveness. 'Mechanical ecology' – the study of organisms in their natural habitat with a biomechanical perspective - is not only important to elucidate adaptations of organisms, but also allows a broader search for new phenomena and organisms that could serve as inspiration for biomimetics.

Mechanical ecology of insect-plant interactions

Plants consist of over 80% of water, but unlike water, many plant secretions have non-Newtonian, viscoelastic properties. Examples are the trap fluids of many tropical pitcher plants (Nepenthes), where viscoelasticity has been shown to aid prey capture and retention. Measuring the viscoelasticity of pitcher fluids accurately requires in situ rheometry, in the tropical field locations where these plants grow, because the fluid properties degrade rapidly in storage. With an interdisciplinary team of biologists and engineers, we designed a portable extensional rheometer that weighs less than 1kg and can be dismantled into parts for easy transport. We used this device to characterize trap fluids of two pitcher plant species: N. rafflesiana in Brunei, Northern Borneo, and N. pervillei in the Seychelles. Viscoelastic behaviour, quantified as the relaxation time after rapid stretching of a small quantity of fluid, appeared relatively late during trap development (before opening), and dropped off sharply around two to three weeks after trap opening. Our results show that fluid properties are highly dynamic over the lifespan of a pitcher trap, with times of maximum fluid viscoelasticity coinciding with times of high attractiveness and prey capture efficiency.

A portable field rheometer reveals age-dependent changes of viscoelastic trap fluids in carnivorous plants

Animal closing forces such as bite and pinch forces may determine access to food and mates and are therefore important performance metrics related to fitness. However, despite the diversity and ecological importance of smaller animals such as many crustaceans and insects, knowledge on the predictors and evolution of closing forces in these taxa is extremely scarce. Here we present a mobile and light-weight closing force measurement setup that is tailored to measure closing forces of a wide range of animals, especially smaller taxa, and an R package for analysing the measurements. During a measurement, in vivo closing forces are converted to an electrical signal by a highly sensitive piezoelectric force transducer. The transducer is housed in a setup that can be manufactured with a 3D printer and generic parts, and the electric signal is amplified by a custom charge amplifier. The R package automatically extracts maximum force values and individual force curves for further curve shape analyses. The shape of these curves may yield information on the underlying biomechanics, physiology, and behaviour during biting/pinching, and has only rarely been studied. We think that the new measurement setup, its ease of use, reproducible components, and fast assembly will enable rapid force measurements in the field and in the lab. In combination with the R package, it will facilitate research on the micro- and macroevolution of animal closing forces in a wide range of taxa, especially in smaller vertebrates and the megadiverse arthropods.

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

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