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Among-species comparisons have been a mainstay of comparative, ecological, and evolutionary physiology for many decades. The ongoing collation of trait databases coupled with the widespread adoption of phylogenetic comparative methods has created fertile ground for the demonstration of new patterns, and for the re-examination of well-known patterns. However, the increases in data richness and analytical sophistication have not changed the fundamental limitations of correlational approaches. Here I explore these limitations, focussing on the important differences between congruence, correlation, and causation. I then use multivariate phylogenetic mixed models to demonstrate the limited extent to which among-species patterns can be used to infer the within-species processes that generate them.

SEB Annual Conference 2022

What meta-analyses and comparative analyses can, and can&#39;t, tell us about biological phenomena

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.

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.

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 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

What meta-analyses and comparative analyses can, and can't, tell us about biological phenomena

technical paper

Life history theory typically considers the costs of reproduction in terms of energy content to released offspring (often measured as clutch mass at birth), yet direct reproductive costs are actually accrued by the mother during the offspring production and provisioning phase. While female body size is well recognised as a strong predictor of clutch mass, remarkably, there is no consensus on how the total energetic costs of reproduction should relate to adult size, nor whether the type of offspring produced (egg or live-young) can modify these relationships. We compiled estimates of body size and metabolism (i.e., reproductive costs) across gravid and non-gravid females, as well as species-specific estimates of clutch mass, for ~80 ectotherm species spanning ~10 orders of magnitude in body size, from rotifer to python. Reproductive cost scaling was hypoallometric – larger species had less reproductive costs relative to their body size than smaller species. Furthermore, species that produced heavier clutches also had relatively less costs than species that produced lighter clutches. Surprisingly, these patterns were congruent across reproductive modes implying that metabolic demands of viviparous and oviparous offspring may change dramatically once released from the mother.

Reproductive metabolism scaling across ectotherms

Time integrated Field Metabolic Rate (FMR) is arguably the most ecologically relevant measure of the energetics of wild animals, but the relative complexity of determining FMR routinely means that we have relatively few large datasets describing variation in energy use in free-living wild animals, particularly for aquatic ectotherms where double labelled water methods cannot be used.
Emerging proxies based on stable isotope systematics associated with respiration allow retrospective estimation of time integrated field metabolic rate, experienced temperature and growth in any free living marine teleost fish. We have estimated FMR in over 1000 individual fish, across nearly 100 species. Here we draw on our data compilation to explore predictions for two contentious topics in fish ecophysiology:
(1) Metabolic cold adaptation: We show that polar species have higher FMR than temperate but not tropical species at equivalent body sizes and temperatures, and that, within species, populations at the cold edge of the range express higher FMR but lower growth rates than populations at the warm edge of the species range.
(2) Gill oxygen limitation theory: FMR data covering 4 orders of magnitude body size within single species show no strong evidence for reduction in metabolic capacity at large body sizes as predicted by the GOLT.











Field metabolic rates of wild marine fishes: reviewing old questions with new data.

The physiological benefits of exercise can be profound. Across the animal kingdom, exercise has been shown to improve locomotor performance and growth, increase brain plasticity and cognition, enhance resistance to disease, and even heighten tolerance to various environmental stressors. In aquaculture particularly, forced exercise is seen as tool to promote the productivity and welfare of fish. Yet, physiological changes following periods of exercise training can be small and context dependent. Experimental evidence has failed to reach a consensus on the mechanisms driving the physiological benefits of forced exercise in fish, particularly because the use of varying of species, life stages, and training regimes can muddy interpretations and because of the limited statistical power that any one individual study holds. We shed light on the physiological benefits of forced exercise in fish by compiling data from published literature. We focus on common physiological traits, such as metabolism, swimming performance, and growth, that are beneficial to wild and captive fishes. Using meta-analytical tools, we capture between-study heterogeneity that allows for stronger predictions on the physiological benefits of exercise training for aquaculture. Exercise training remains an exciting management prospect for the culture of ‘fitter’ fish that is strengthened by this new holistic understanding.

Farming fitter fish through forced exercise: A meta-analysis

The surface of pant leaves hosts a huge diversity of interacting ectotherms. The ecophysiology of these tiny organisms, as well as the rate of biotic interactions, depends on the leaf surface temperature. Most of these organisms are tiny enough to be totally submerged within the leaf boundary layer, making them largely under the influence of the leaf functioning. The temperature of a leaf surface can deviate from air temperature sometimes quite strongly. In this presentation, I will detail the biophysical mechanisms determining the microclimate of arthropods living at the leaf surface. A comprehensive understanding of the leaf-air temperature deviations as well as the temperature heterogeneity at the within-leaf surface scale, is important to identify the extent to which ectotherms can exploit these thermal patterns to thermoregulate. Then, arthropod herbivore can fundamentally modify the functioning of the leaf when feeding on it; these changes have cascading effects on the leaf microclimate. These cascading effects can help explain the patterns of thermal adaptation among arthropod herbivores and predict the consequences of competitive interactions. These approaches needs to be cross-scales since the fine-scale microclimate is embedded into another microclimate at larger scale. Finally, the leaf microclimate can be placed in the context of climate change impacts: will the leaf surface provide ectotherms with a buffer of extreme heat or by contrast will it magnify the atmospheric changes? This knowledge of the leaf microclimate helps us determining the vulnerability of arthropods to warming.

The role of microclimate at fine scales in driving exposure of ectotherms to climate change: integrating biophysics, physiology and ecology

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.

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

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.

What meta-analyses and comparative analyses can, and can't, tell us about biological phenomena

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