Czechia

The physiological response to thermal fluctuations has been a subject of investigation for decades. These studies have been fundamental in unraveling the underlying mechanisms that allow organisms to cope with temperature variations. However, when attempting to generalize organism responses to environmental changes in natural settings, we confront the inconvenient truth: the natural environment is inherently complex, characterized by diverse and variable stressors. To address this complexity, a transition from a single stressor approach to a multiple stressor scenario becomes essential. We must explore how different thermal fluctuations interact with co-variability in other environmental factors, shaping the phenotypic responses of wild organisms. While recent research has focused on predictable co-variation between stressors (e.g., heat and hypoxia), the effects of simultaneous exposure to emerging and human-driven environmental changes—such as heatwaves and toxicant releases—remain unclear. In this context, I present two case studies examining the phenotypic plasticity of thermal tolerance in adult and offspring generations of two fish species. Specifically, we investigate their responses to environmentally relevant concentrations of copper, a widely used and released metal, both independently and in conjunction with a heatwave event. Contrary to our initial hypothesis, the data revealed unexpected results: thermal plasticity was not negatively affected by copper exposure, to some extent. Instead, we observed a potential cross-tolerance effect. This suggests that exposure to one stressor may enhance an organism’s ability to cope with a second stressor. These findings offer new perspectives and inform future research directions.

SEB Conference 2024

One is not enough: the importance of multiple-stressor scenarios in thermal plasticity studies

phenotypic plasticity

cross-tolerance

thermal tolerance

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Teleosts maintain body fluid ionic and acid-base homeostasis through energy-consuming ion transport mechanisms in the gills and other organs. Our serial studies identified a new gill cell type (GR cells) in zebrafish and tilapia, which are rich in glycogen and provide glucose or lactate/pyruvate to neighboring ionocytes. Different types of glucose and monocarboxylate transporters were found to facilitate energy deposition and supply between ionocytes and GR cells. On the other hand, ammonotelic fishes are suggested to rely on ammonia excretion to enhance net acid secretion because ammoniogenesis produces HCO3- to facilitate body fluid acid-base homeostasis. We recently extended our study to understand how ammoniagenesis occurs and is coordinated with ammonia excretion in fish gills. In medaka and other species, we have discovered an undiscovered ammonia-producing cell type that is rich in glutaminase (GLS cells) and located adjacent to the ammonia-excreting ionocytes (NHE cells) in the gills. The unique division of labor between GLS and NHE cells in the gills allows medaka to simultaneously upregulate GLS activity and ammonia excretion shortly after exposure to acidic environments. These findings provide fundamental information to enhance our mechanistic understanding of the energy metabolism underpinning gill ion transport functions and the related physiological adaptations of vertebrates during evolution.



Ion regulation and related energy metabolism in fish gills

Embryonic Gulf killifish (Fundulus grandis) exhibit precocial parasympathetic-mediated cardiac control, yet little there is little research concerning their unusually early vagal tone. These embryos feature traits uniquely suited for studying early ANS development as 1) they require no anesthesia, thereby eliminating collateral interference that anesthetics have on the ANS or cardiovascular system, 2) feature a semi-transparent chorion, enabling direct observation of the heart, and 3) possess a fully sequenced and annotated genome conducive to understanding genotype-phenotype relationships. Parasympathetic inhibition of the heart created by a ‘startle’ response is evident as a transient cardiac arrest and can be performed by applying gentle mechanical pressure to the embryos under a glass microscope slip, followed by atropine administration upon positive observation of vagal tone. Habituation assays were performed to determine whether an attenuated vagal response to repeated startle stimuli emerged over time, a further expression of early cardiac control. This included obtaining trace data of cardiac activity using a high-throughput heart monitor system for fish embryos. At 80% to hatch a startle stimulus induces transient bradycardia for ~30-40sec. This parasympathetic response was blocked by 1 mmol atropine. Cardiac activity observed during habituation assays showed a non-diminished susceptibility to induced bradycardia. Embryos as young as 60-70% to hatch (~9 days post-fertilization) exhibit vagal tone through parasympathetic stimulation, signifying the initial vagal innervation of the heart. Exploiting this precocial onset of parasympathetic innervation in Gulf killifish embryos can serve as an interface linking established genotypes to relevant physiological phenotypes.

Onset of Cardiovascular Regulation by Vagal Innervation of the Heart in Embryonic Gulf Killifish Embryos (Fundulus grandis)

The ability to perform sit-to-stand (STS) behaviours is fundamental for humans and other animals, yet the underlying high-level control goal driving the selection of a specific movement pattern for the STS transition remains elusive. Exploring the STS transition in non-human animals, particularly birds, offers an opportunity to deepen this understanding and allows for an independent assessment of how body sizes influence performance criteria. Computational biomechanical modelling and simulation, combined with optimal control methods, provide a rigorous and mechanistic approach to address these questions, offering insights that experimental limitations may hinder. Drawing inspiration from human studies, we systematically evaluate STS performance criteria (e.g., minimisation of effort and the muscle force rate) and examine how these criteria vary with body sizes, using a simplified two-link model to simulate vertical movements. We use this simplified simulation to inform fully predictive, three-dimensional, muscle-driven simulations of the STS transition in the emu (Dromaius novaehollandiae), a large bipedal bird. This study, focusing on emus, provides insights into avian species’ control strategies during the STS transition, with future investigations extending to simulate this transition in other bird species, contributing not only to our understanding of organismal morphofunctional specialisation but also to applications in robotics, prosthetics, and animal welfare, as well as aiding in the reconstruction of locomotion in extinct species.

Predictive simulations of musculoskeletal function and sit-to-stand performance in a large bipedal bird - the emu (Dromaius novaehollandiae)

Chromosomal fusions have been hypothesized to facilitate evolutionary adaptation, but empirical evidence has been scarce. We examined patterns of genome evolution in the copepod Eurytemora affinis species complex, which are numerically dominant and highly invasive, with the extraordinary capacity to rapidly invade novel salinities. Prior studies from my laboratory (Lee Lab) revealed parallel selection acting on the same sets of ion transporter genes during independent saline to freshwater invasions by populations from genetically distinct clades. Our chromosome-level genomes of three genetically divergent clades of this species complex revealed peculiar genome architectures that might contribute to their remarkable capacity to acclimate and evolve during salinity invasions. Among the three genetically distinct clades of E. affinis complex, we discovered independent chromosomal fusions in two different clades, with the Europe clade (E. affinis proper) having 15 chromosomes, fusing independently into 7 chromosomes in the Gulf clade (E. gulfia) and 4 chromosomes in the Atlantic clade (E. carolleeae). Notably, for the highly invasive Atlantic clade (E. carolleeae), chromosomal fusion sites, especially the centromeres, were significantly enriched with signatures of selection associated with contemporary shifts from saline to freshwater habitats. These chromosomal fusions joined functionally-related ion transporter genes, forming "supergenes" at the centromeres, where recombination is low. This study uncovers novel patterns of genome architecture evolution with potentially important implications for mechanisms of adaptive evolution in response to radical environmental change.

Genome Architecture Evolution in the copepod Eurytemora affinis species complex

Large-scale comparative genomics studies offer valuable resources for understanding both functional and evolutionary rate constraints. It is suggested that constraint aligns with the topology of genomic protein-protein interaction (PPI) networks, increasing toward the center, with intermediate nodes combining relaxed constraint with higher contributions to the phenotype due to pleiotropy. However, this pattern has yet to be demonstrated in vertebrates. Here I show that constraint intensifies toward the network's center in both yeast and placental mammals. Genes with rate changes associated with emergence of mammalian hibernation cluster mostly toward intermediate positions, with higher constraint in faster-evolving genes, which is indicative of a “sweet spot” for adaptation. Network node metrics could therefore predict genomic regions favored for adaptation even in clades lacking empirical constraint data. To explore this idea, I used lacertid lizards as example for such group of species without empirical constraint data, and show that genes with signatures of selection in response to a latitudinal environmental gradient likewise cluster in more intermediate positions, which is even more pronounced in genes which have been re-used for this purpose independently multiple times across vertebrates. These particular genes further reveal a strong correlation between evolutionary rate and preference for cooler environments, affirming prior results that the diversification of lacertid lizards is predominantly driven by adaptation to cooler climates. In conclusion, genome architecture offers important clues about the co-evolution of protein-coding genes that respond to environmental stimuli, thereby enhancing our comprehension of the resilience and adaptability of organisms in the face of climate change.


Linking network topology, evolutionary constraint, and abiotic environmental adaptation

Protein-protein interaction (PPI) network topology determines properties of genes, such as expression levels, or levels of evolutionary constraint. When genes are central to a network they are more likely to be conserved and highly expressed, whereas genes that are able to change in response to evolutionary pressures but expressed at lower levels are located on the periphery of the network. We used transcriptomic data of zebrafish (Danio rerio) embryos to compare the PPI properties of the response to two environmental stressors (heat, UVR and combination). We show that genes with stress response Gene Ontology are situated centrally to the PPI network. The transcriptomic response to heat occupied central and peripheral positions within the reference network, whereas UV response occupied central and intermediate positions. Prefacing UVR with heat led to a downshift of DEGs, which could explain the hormetic effect of heat stress. In addition, when only considering genes specific to each stressor, heat responsive DEGs were located more peripherally, and uniquely UV responsive DEGs were located intermedially in the PPI. Overall, these results support the idea that the stress response must have both conserved and derived aspects, in order to respond to stress generally but to also allow for specialisation, which we show to be reflected in the PPI network architecture. These properties can aid in better understanding the organismal response to diverse and co-occurring environmental stressors.

The protein-protein interaction network architecture of the environmental stress response in zebrafish embryos

Fishes are fantastically plastic creatures, capable of altering their morphology, physiology, life-history, and even offspring responses to changes in the environment. A key question in freshwater ecology is how fishes will respond through plasticity to continued changes in climate - especially to predicted increases in the variability of temperature. Here, we describe lessons learned from long-term, multi-generational experiments examining thermal variability's plastic effects in a model organism, zebrafish (Danio rerio). We found that long-term exposure to thermal variability confers relative benefits in a number of fitness-related traits, but these benefits were not without costs. We highlight the advantages of using thermally variable regimes in experiments and discuss important knowledge gaps that remain in the study of thermal variability and plasticity.

Plasticity to thermal variability within and across generations

Core body temperature (Tc) is increasingly used as a biomarker of the fitness of an animal to its environment. Periodogram and cosinor analysis can be used to estimate the characteristics of the circadian rhythm of Tc. The sampling interval can be manipulated to maximise the recording period of loggers, but the impact of interval on the output of periodogram or cosinor analysis is unknown. Basic guidelines are available from signal analysis theory, but have never been tested on Tc data. We obtained data at 1-, 5-, or 10-minute intervals from nine avian or mammalian species, and re-sampled those data to simulate logging at up to 240-minute interval. The period of the rhythm was first analysed using the Lomb-Scargle periodogram, and the mesor, amplitude, acrophase, and adjusted coefficient of determination (R2) from the original and the re-sampled data were obtained using cosinor analysis. Sampling intervals longer than 60 minutes did not affect the average mesor, amplitude, acrophase, or adjusted R2, but did impact the period of the rhythm. In most species, the period was not detectable when intervals longer than 120 minutes were used. In all individual profiles, a 30-minute sampling interval modified the values of the mesor and amplitude by less than 0.1°C, and the adjusted R2 by less than 0.1. At a 30-minute interval, the acrophase was accurate to within 15 minutes for all species except mice. In most cases, a 30-minute sampling interval provides a reliable balance between parameter accuracy and logger longevity.

Optimal sampling interval for characterisation of the circadian rhythm of body temperature in homeothermic animals using periodogram and cosinor analysis

Improving crop intrinsic water use efficiency (iWUE) usually comes at the expense of carbon assimilation. Sorghum is a key crop in many vulnerable agricultural systems with higher tolerance to water stress (WS) than other crops. To investigate physiological controls on iWUE and its inheritance in sorghum we screened 90 genotypes selected based on inherited haplotypes from an elite or five exotics lines, which included different aquaporin (AQP) alleles. We found significant variation among key highly heritable gas exchange and hydraulic traits. Plants with a higher proportion of the non-stomatal component of iWUE still maintained iWUE under WS by maintaining photosynthetic capacity, independently of reduction in leaf hydraulic conductance. Haplotypes associated with two AQPs (SbPIP1.1 and SbTIP3.2) influenced iWUE and related traits. These findings expand the range of traits that bridge the trade-off between iWUE and productivity in C4 crops, and provide possible genetic regions that can be targeted for breeding.

Hydraulic and stomatal controls on water use efficiency in a sorghum sub-population with varying aquaporin alleles

Quantifying trade-offs between life history traits is complex. In particular, the extent of trade-offs between reproduction and somatic maintenance remains difficult to quantify in wild animals. Using the dynamic nature of telomeres may help to elucidate this process. Telomere length (TL) is generally associated with longevity, as it tends to shorten with age, and can thus serve as a biomarker associated with future survival. However, TL varies widely among individuals within a population, as it can be influenced by individual and environmental factors. An increased reproductive effort appears to accelerate telomere erosion, making TL a potential biomarker to describe the trade-off between reproduction and future survival. On the other hand, TL partially explains individual performance, with longer telomeres being associated with higher reproductive success.
This study investigates the factors contributing to TL variation among female Tree swallows (Tachycineta bicolor) from a wild population in southern Québec, Canada. Specifically, it assesses the effects of individual (ex. age, reproductive traits) and environmental (ex. habitat quality, density) factors on TL variation within and between females over the course of a breeding season in this species. Our results improve our understanding of telomere dynamics in wildlife populations and their potential use as biomarkers of reproductive performance.

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Ion regulation and related energy metabolism in fish gills

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Context-dependence of thermal plasticity in insects

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