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Metabolic rate, the rate of energy use, underpins key ecological traits of organisms, from development and locomotion to interaction rates between individuals. In a warming world, the temperature-dependence of metabolic rate is anticipated to shift predator-prey dynamics. Yet, there is little real-world evidence on the effects of warming on trophic interactions. We measured the respiration rates of aquatic larvae of three insect species from populations experiencing a natural temperature gradient in a large-scale mesocosm experiment. Using a mechanistic model we predicted the effects of warming on these taxa's predator-prey interaction rates. We found that species-specific differences in metabolic plasticity lead to mismatches in the temperature-dependence of their relative velocities, resulting in altered predator-prey interaction rates. This study underscores the role of metabolic plasticity at the species level in modifying trophic interactions and proposes a mechanistic modelling approach that allows an efficient, high-throughput estimation of climate change threats across species pairs.
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Mudança Climática , Cadeia Alimentar , Comportamento Predatório , Animais , Larva/fisiologia , Temperatura , Especificidade da Espécie , Insetos/fisiologiaRESUMO
Our understanding of how microbes respond to micropollutants, such as pesticides, is almost wholly based on single-species responses to individual chemicals. However, in natural environments, microbes experience multiple pollutants simultaneously. Here we perform a matrix of multi-stressor experiments by assaying the growth of model and non-model strains of bacteria in all 255 combinations of 8 chemical stressors (antibiotics, herbicides, fungicides and pesticides). We found that bacterial strains responded in different ways to stressor mixtures, which could not be predicted simply from their phylogenetic relatedness. Increasingly complex chemical mixtures were both more likely to negatively impact bacterial growth in monoculture and more likely to reveal net interactive effects. A mixed co-culture of strains proved more resilient to increasingly complex mixtures and revealed fewer interactions in the growth response. These results show predictability in microbial population responses to chemical stressors and could increase the utility of next-generation eco-toxicological assays.
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Poluentes Ambientais , Praguicidas , Filogenia , Praguicidas/toxicidade , Bactérias/genética , Misturas ComplexasRESUMO
The capacity of arthropod populations to adapt to long-term climatic warming is currently uncertain. Here we combine theory and extensive data to show that the rate of their thermal adaptation to climatic warming will be constrained in two fundamental ways. First, the rate of thermal adaptation of an arthropod population is predicted to be limited by changes in the temperatures at which the performance of four key life-history traits can peak, in a specific order of declining importance: juvenile development, adult fecundity, juvenile mortality and adult mortality. Second, directional thermal adaptation is constrained due to differences in the temperature of the peak performance of these four traits, with these differences expected to persist because of energetic allocation and life-history trade-offs. We compile a new global dataset of 61 diverse arthropod species which provides strong empirical evidence to support these predictions, demonstrating that contemporary populations have indeed evolved under these constraints. Our results provide a basis for using relatively feasible trait measurements to predict the adaptive capacity of diverse arthropod populations to geographic temperature gradients, as well as ongoing and future climatic warming.
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Artrópodes , Características de História de Vida , Animais , Temperatura , Aclimatação , FenótipoRESUMO
Movement facilitates and alters species interactions, the resulting food web structures, species distribution patterns, community structures and survival of populations and communities. In the light of global change, it is crucial to gain a general understanding of how movement depends on traits and environmental conditions. Although insects and notably Coleoptera represent the largest and a functionally important taxonomic group, we still know little about their general movement capacities and how they respond to warming. Here, we measured the exploratory speed of 125 individuals of eight carabid beetle species across different temperatures and body masses using automated image-based tracking. The resulting data revealed a power-law scaling relationship of average movement speed with body mass. By additionally fitting a thermal performance curve to the data, we accounted for the unimodal temperature response of movement speed. Thereby, we yielded a general allometric and thermodynamic equation to predict exploratory speed from temperature and body mass. This equation predicting temperature-dependent movement speed can be incorporated into modeling approaches to predict trophic interactions or spatial movement patterns. Overall, these findings will help improve our understanding of how temperature effects on movement cascade from small to large spatial scales as well as from individual to population fitness and survival across communities.
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There are many ways in which methods and theories from physics can and have been applied to biology and ecology. The oldest example is the application of classical mechanics to animal movement (biomechanics), from tiny bacteria to massive whales. This application is intuitive: most people when observing an elephant lumber along would be happy to conclude that animals are machines in that they are so obviously made of moving parts designed to perform work (in its physical sense) under the constraints of elementary forces (predominantly gravity if you were an elephant!). Indeed, the potential for this link between physics and biology was foreseen by Aristotle around 2000 years before the mathematical bases of classical mechanics were founded (Nussbaum 1986).
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Fenômenos Biomecânicos , Ecossistema , Animais , Ecologia , Elefantes , FísicaRESUMO
Respiratory release of CO2 by microorganisms is one of the main components of the global carbon cycle. However, there are large uncertainties regarding the effects of climate warming on the respiration of microbial communities, owing to a lack of mechanistic, empirically tested theory that incorporates dynamic species interactions. We present a general mathematical model which predicts that thermal sensitivity of microbial community respiration increases as species interactions change from competition to facilitation (for example, commensalism, cooperation and mutualism). This is because facilitation disproportionately increases positive feedback between the thermal sensitivities of species-level metabolic and biomass accumulation rates at warmer temperatures. We experimentally validate our theoretical predictions in a community of eight bacterial taxa and show that a shift from competition to facilitation, after a month of co-adaptation, caused a 60% increase in the thermal sensitivity of respiration relative to de novo assembled communities that had not co-adapted. We propose that rapid changes in species interactions can substantially change the temperature dependence of microbial community respiration, which should be accounted for in future climate-carbon cycle models.
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Bactérias , Microbiota , Temperatura , Biomassa , Bactérias/genética , RespiraçãoRESUMO
How complex microbial communities respond to climatic fluctuations remains an open question. Due to their relatively short generation times and high functional diversity, microbial populations harbor great potential to respond as a community through a combination of strain-level phenotypic plasticity, adaptation, and species sorting. However, the relative importance of these mechanisms remains unclear. We conducted a laboratory experiment to investigate the degree to which bacterial communities can respond to changes in environmental temperature through a combination of phenotypic plasticity and species sorting alone. We grew replicate soil communities from a single location at six temperatures between 4°C and 50°C. We found that phylogenetically and functionally distinct communities emerge at each of these temperatures, with K-strategist taxa favored under cooler conditions and r-strategist taxa under warmer conditions. We show that this dynamic emergence of distinct communities across a wide range of temperatures (in essence, community-level adaptation) is driven by the resuscitation of latent functional diversity: the parent community harbors multiple strains pre-adapted to different temperatures that are able to 'switch on' at their preferred temperature without immigration or adaptation. Our findings suggest that microbial community function in nature is likely to respond rapidly to climatic temperature fluctuations through shifts in species composition by resuscitation of latent functional diversity.
Most ecosystems on Earth rely on dynamic communities of microorganisms which help to cycle nutrients in the environment. There is increasing concern that climate change may have a profound impact on these complex networks formed of large numbers of microbial species linked by intricate biochemical relationships. Any species within a microbial community can acclimate to new temperatures by quickly tweaking their biological processes, for example by activating genes that are more suited to warmer conditions. Over time, a species may acclimate or adapt to new conditions. However, the community as a whole can also respond to these changes, and often much faster, by simply altering the abundance or presence of its members through a process known as species sorting. It remains unclear exactly how acclimation, adaptation and species sorting each contribute to the community's response to a temperature shift an increasingly common scenario under global climate change. To address this question, Smith et al. investigated how species sorting and acclimation may help whole soil bacterial communities to cope with lasting changes in temperature. To do so, soil samples from a single field site (and therefore featuring the same microbial community) were incubated for four weeks under six different temperatures. Genetic analyses revealed that, at the end of the experiments, distinct communities specific to a given temperature had emerged. They all differed in species composition and the types of biological functions they could perform. Further experiments showed that each community had been taken over by strains of bacteria which grew best at the new temperature that they had been exposed to, including extreme warming scenarios never seen in their native environment. This suggests that these organisms were already present in the original community. They had persisted even under temperatures which were not optimal for them, acting as a slumbering ('latent') 'reservoir' of traits and functional abilities that allowed species sorting to produce distinct and functionally capable communities in each novel thermal environment. This suggests that species sorting could help bacterial communities to cope with dramatic changes in their thermal environment. Smith et al.'s findings suggest that bacterial communities can cope with warming environments much better than has been previously thought. In the future, this work may help researchers to better predict how climate change could impact microbial community structure and functioning, and most crucially their contributions to the global carbon cycle.
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Microbiota , Temperatura , Aclimatação , Adaptação Fisiológica , SoloRESUMO
Microbes play a primary role in aquatic ecosystems and biogeochemical cycles. Spatial patchiness is a critical factor underlying these activities, influencing biological productivity, nutrient cycling and dynamics across trophic levels. Incorporating spatial dynamics into microbial models is a long-standing challenge, particularly where small-scale turbulence is involved. Here, we combine a fully 3D direct numerical simulation of convective mixed layer turbulence, with an individual-based microbial model to test the key hypothesis that the coupling of gyrotactic motility and turbulence drives intense microscale patchiness. The fluid model simulates turbulent convection caused by heat loss through the fluid surface, for example during the night, during autumnal or winter cooling or during a cold-air outbreak. We find that under such conditions, turbulence-driven patchiness is depth-structured and requires high motility: Near the fluid surface, intense convective turbulence overpowers motility, homogenising motile and non-motile microbes approximately equally. At greater depth, in conditions analogous to a thermocline, highly motile microbes can be over twice as patch-concentrated as non-motile microbes, and can substantially amplify their swimming velocity by efficiently exploiting fast-moving packets of fluid. Our results substantiate the predictions of earlier studies, and demonstrate that turbulence-driven patchiness is not a ubiquitous consequence of motility but rather a delicate balance of motility and turbulent intensity.
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Ecossistema , NataçãoRESUMO
Organisms have the capacity to alter their physiological response to warming through acclimation or adaptation, but the consequence of this metabolic plasticity for energy flow through food webs is currently unknown, and a generalisable framework does not exist for modelling its ecosystem-level effects. Here, using temperature-controlled experiments on stream invertebrates from a natural thermal gradient, we show that the ability of organisms to raise their metabolic rate following chronic exposure to warming decreases with increasing body size. Chronic exposure to higher temperatures also increases the acute thermal sensitivity of whole-organismal metabolic rate, independent of body size. A mathematical model parameterised with these findings shows that metabolic plasticity could account for 60% higher ecosystem energy flux with just +2 °C of warming than a traditional model based on ecological metabolic theory. This could explain why long-term warming amplifies ecosystem respiration rates through time in recent mesocosm experiments, and highlights the need to embed metabolic plasticity in predictive models of global warming impacts on ecosystems.
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Ecossistema , Aquecimento Global , Animais , Cadeia Alimentar , Invertebrados , TemperaturaRESUMO
Helminth parasites are part of almost every ecosystem, with more than 300 000 species worldwide. Helminth infection dynamics are expected to be altered by climate change, but predicting future changes is difficult owing to lacking thermal sensitivity data for greater than 99.9% of helminth species. Here, we compiled the largest dataset to date on helminth temperature sensitivities and used the Metabolic Theory of Ecology to estimate activation energies (AEs) for parasite developmental rates. The median AE for 129 thermal performance curves was 0.67, similar to non-parasitic animals. Although exceptions existed, related species tended to have similar thermal sensitivities, suggesting some helminth taxa are inherently more affected by rising temperatures than others. Developmental rates were more temperature-sensitive for species from colder habitats than those from warmer habitats, and more temperature sensitive for species in terrestrial than aquatic habitats. AEs did not depend on whether helminth life stages were free-living or within hosts, whether the species infected plants or animals, or whether the species had an endotherm host in its life cycle. The phylogenetic conservatism of AE may facilitate predicting how temperature change affects the development of helminth species for which empirical data are lacking or difficult to obtain.
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Helmintos , Parasitos , Animais , Ecossistema , Helmintos/fisiologia , Interações Hospedeiro-Parasita/fisiologia , FilogeniaRESUMO
Mathematical models that incorporate the temperature dependence of lab-measured life history traits are increasingly being used to predict how climatic warming will affect ectotherms, including disease vectors and other arthropods. These temperature-trait relationships are typically measured under laboratory conditions that ignore how conspecific competition in depleting resource environments-a commonly occurring scenario in nature-regulates natural populations. Here, we used laboratory experiments on the mosquito Aedes aegypti, combined with a stage-structured population model, to investigate this issue. We find that intensified larval competition in ecologically-realistic depleting resource environments can significantly diminish the vector's maximal population-level fitness across the entire temperature range, cause a ~6 °C decrease in the optimal temperature for fitness, and contract its thermal niche width by ~10 °C. Our results provide evidence for the importance of considering intra-specific competition under depleting resources when predicting how arthropod populations will respond to climatic warming.
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Aedes/genética , Aptidão Genética , Temperatura , Aedes/crescimento & desenvolvimento , Animais , Larva/genética , Larva/crescimento & desenvolvimento , Mosquitos Vetores/genética , Mosquitos Vetores/crescimento & desenvolvimentoRESUMO
Non-equilibrium thermodynamics has long been an area of substantial interest to ecologists because most fundamental biological processes, such as protein synthesis and respiration, are inherently energy-consuming. However, most of this interest has focused on developing coarse ecosystem-level maximisation principles, providing little insight into underlying mechanisms that lead to such emergent constraints. Microbial communities are a natural system to decipher this mechanistic basis because their interactions in the form of substrate consumption, metabolite production, and cross-feeding can be described explicitly in thermodynamic terms. Previous work has considered how thermodynamic constraints impact competition between pairs of species, but restrained from analysing how this manifests in complex dynamical systems. To address this gap, we develop a thermodynamic microbial community model with fully reversible reaction kinetics, which allows direct consideration of free-energy dissipation. This also allows species to interact via products rather than just substrates, increasing the dynamical complexity, and allowing a more nuanced classification of interaction types to emerge. Using this model, we find that community diversity increases with substrate lability, because greater free-energy availability allows for faster generation of niches. Thus, more niches are generated in the time frame of community establishment, leading to higher final species diversity. We also find that allowing species to make use of near-to-equilibrium reactions increases diversity in a low free-energy regime. In such a regime, two new thermodynamic interaction types that we identify here reach comparable strengths to the conventional (competition and facilitation) types, emphasising the key role that thermodynamics plays in community dynamics. Our results suggest that accounting for realistic thermodynamic constraints is vital for understanding the dynamics of real-world microbial communities.
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Microbiota/fisiologia , Modelos Biológicos , Trifosfato de Adenosina/biossíntese , Biodiversidade , Biologia Computacional , Simulação por Computador , Ecossistema , Metabolismo Energético , Cinética , Proteoma/metabolismo , TermodinâmicaRESUMO
New microbial communities often arise through the mixing of two or more separately assembled parent communities, a phenomenon that has been termed "community coalescence". Understanding how the interaction structures of complex parent communities determine the outcomes of coalescence events is an important challenge. While recent work has begun to elucidate the role of competition in coalescence, that of cooperation, a key interaction type commonly seen in microbial communities, is still largely unknown. Here, using a general consumer-resource model, we study the combined effects of competitive and cooperative interactions on the outcomes of coalescence events. To do so, we simulate coalescence events between pairs of communities with different degrees of competition for shared carbon resources and cooperation through cross-feeding on leaked metabolic by-products (facilitation). We also study how structural and functional properties of post-coalescence communities evolve when they are subjected to repeated coalescence events. We find that in coalescence events, the less competitive and more cooperative parent communities contribute a higher proportion of species to the new community because of their superior ability to deplete resources and resist invasions. Consequently, when a community is subjected to repeated coalescence events, it gradually evolves towards being less competitive and more cooperative, as well as more speciose, robust and efficient in resource use. Encounters between microbial communities are becoming increasingly frequent as a result of anthropogenic environmental change, and there is great interest in how the coalescence of microbial communities affects environmental and human health. Our study provides new insights into the mechanisms behind microbial community coalescence, and a framework to predict outcomes based on the interaction structures of parent communities.
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Interações Microbianas/fisiologia , Microbiota/fisiologia , Modelos Biológicos , Evolução Biológica , Biologia Computacional , Simulação por Computador , Humanos , Conceitos MatemáticosRESUMO
Laboratory-derived temperature dependencies of life-history traits are increasingly being used to make mechanistic predictions for how climatic warming will affect vector-borne disease dynamics, partially by affecting abundance dynamics of the vector population. These temperature-trait relationships are typically estimated from juvenile populations reared on optimal resource supply, even though natural populations of vectors are expected to experience variation in resource supply, including intermittent resource limitation. Using laboratory experiments on the mosquito Aedes aegypti, a principal arbovirus vector, combined with stage-structured population modelling, we show that low-resource supply in the juvenile life stages significantly depresses the vector's maximal population growth rate across the entire temperature range (22-32°C) and causes it to peak at a lower temperature than at high-resource supply. This effect is primarily driven by an increase in juvenile mortality and development time, combined with a decrease in adult size with temperature at low-resource supply. Our study suggests that most projections of temperature-dependent vector abundance and disease transmission are likely to be biased because they are based on traits measured under optimal resource supply. Our results provide compelling evidence for future studies to consider resource supply when predicting the effects of climate and habitat change on vector-borne disease transmission, disease vectors and other arthropods.
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Aedes , Mosquitos Vetores , Animais , Vetores de Doenças , Aptidão Genética , TemperaturaRESUMO
Multiple stressors, such as warming and invasions, often occur together and have nonadditive effects. Most studies to date assume that stressors operate in perfect synchrony, but this will rarely be the case in reality. Stressor sequence and overlap will have implications for ecological memory - the ability of past stressors to influence future responses. Moreover, stressors are usually defined in an anthropocentric context: what we consider a short-term stressor, such as a flood, will span multiple generations of microbes. We argue that to predict responses to multiple stressors from individuals to the whole ecosystem, it is necessary to consider metabolic rates, which determine the timescales at which individuals operate and therefore, ultimately, the ecological memory at different levels of ecological organization.
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Ecossistema , HumanosRESUMO
Bach et al. [1] recently presented an algorithm for constructing confluent drawings, by leveraging power graph decomposition to generate an auxiliary routing graph. We identify two issues with their method which we call the node split and short-circuit problems, and solve both by modifying the routing graph to retain the hierarchical structure of power groups. We also classify the exact type of confluent drawings that the algorithm can produce as 'power-confluent', and prove that it is a subclass of the previously studied 'strict confluent' drawing. A description and source code of our implementation is also provided, which additionally includes an improved method for power graph construction.
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How species coexistence (mathematical 'feasibility') in food webs emerges from species' trophic interactions remains a long-standing open question. Here we investigate how structure (network topology and body-size structure) and behaviour (foraging strategy and spatial dimensionality of interactions) interactively affect feasibility in food webs. Metabolically-constrained modelling of food-web dynamics based on whole-organism consumption revealed that feasibility is promoted in systems dominated by large-eat-small foraging (consumers eating smaller resources) whenever (1) many top consumers are present, (2) grazing or sit-and-wait foraging strategies are common, and (3) species engage in two-dimensional interactions. Congruently, the first two conditions were associated with dominance of large-eat-small foraging in 74 well-resolved (primarily aquatic) real-world food webs. Our findings provide a new, mechanistic understanding of how behavioural properties can modulate the effects of structural properties on species coexistence in food webs, and suggest that 'being feasible' constrains the spectra of behavioural and structural properties seen in natural food webs.
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Cadeia Alimentar , Comportamento Predatório , Animais , Tamanho Corporal , Modelos BiológicosRESUMO
Developing a thorough understanding of how ectotherm physiology adapts to different thermal environments is of crucial importance, especially in the face of global climate change. A key aspect of an organism's thermal performance curve (TPC)-the relationship between fitness-related trait performance and temperature-is its thermal sensitivity, i.e., the rate at which trait values increase with temperature within its typically experienced thermal range. For a given trait, the distribution of thermal sensitivities across species, often quantified as "activation energy" values, is typically right-skewed. Currently, the mechanisms that generate this distribution are unclear, with considerable debate about the role of thermodynamic constraints versus adaptive evolution. Here, using a phylogenetic comparative approach, we study the evolution of the thermal sensitivity of population growth rate across phytoplankton (Cyanobacteria and eukaryotic microalgae) and prokaryotes (bacteria and archaea), 2 microbial groups that play a major role in the global carbon cycle. We find that thermal sensitivity across these groups is moderately phylogenetically heritable, and that its distribution is shaped by repeated evolutionary convergence throughout its parameter space. More precisely, we detect bursts of adaptive evolution in thermal sensitivity, increasing the amount of overlap among its distributions in different clades. We obtain qualitatively similar results from evolutionary analyses of the thermal sensitivities of 2 physiological rates underlying growth rate: net photosynthesis and respiration of plants. Furthermore, we find that these episodes of evolutionary convergence are consistent with 2 opposing forces: decrease in thermal sensitivity due to environmental fluctuations and increase due to adaptation to stable environments. Overall, our results indicate that adaptation can lead to large and relatively rapid shifts in thermal sensitivity, especially in microbes for which rapid evolution can occur at short timescales. Thus, more attention needs to be paid to elucidating the implications of rapid evolution in organismal thermal sensitivity for ecosystem functioning.
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Adaptação Fisiológica , Evolução Biológica , Crescimento Demográfico , Temperatura , Bases de Dados como Assunto , Padrões de Herança/genética , Modelos Biológicos , Filogenia , Fitoplâncton/fisiologia , Células Procarióticas/metabolismo , Especificidade da EspécieRESUMO
Many important endemic and emerging diseases are transmitted by vectors that are biting arthropods. The functional traits of vectors can affect pathogen transmission rates directly and also through their effect on vector population dynamics. Increasing empirical evidence shows that vector traits vary significantly across individuals, populations, and environmental conditions, and at time scales relevant to disease transmission dynamics. Here, we review empirical evidence for variation in vector traits and how this trait variation is currently incorporated into mathematical models of vector-borne disease transmission. We argue that mechanistically incorporating trait variation into these models, by explicitly capturing its effects on vector fitness and abundance, can improve the reliability of their predictions in a changing world. We provide a conceptual framework for incorporating trait variation into vector-borne disease transmission models, and highlight key empirical and theoretical challenges. This framework provides a means to conceptualize how traits can be incorporated in vector borne disease systems, and identifies key areas in which trait variation can be explored. Determining when and to what extent it is important to incorporate trait variation into vector borne disease models remains an important, outstanding question.
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To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness-related rates to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can-at least partly-overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta-analysis of the thermal performance curves of growth rate of phytoplankton-a globally important functional group-controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak "hotter-is-better" constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints.