scholarly journals Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints

2018 ◽  
Author(s):  
Dimitrios - Georgios Kontopoulos ◽  
Erik van Sebille ◽  
Michael Lange ◽  
Gabriel Yvon-Durocher ◽  
Timothy G. Barraclough ◽  
...  

AbstractTo 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 traits 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.

2014 ◽  
Vol 62 (6) ◽  
pp. 448 ◽  
Author(s):  
Sophie G. Arnall ◽  
Gerald Kuchling ◽  
Nicola J. Mitchell

Thermal performance curves are useful for predicting how organisms might respond to environmental change, and are becoming increasingly applicable for ectothermic animals threatened by climate change. Here we present a thermal performance curve for the critically endangered western swamp turtle (Pseudemydura umbrina) based upon measurements of O2 consumption and CO2 production obtained by flow-through respirometry at temperatures between 15 and 30°C. Standard metabolic rate was significantly higher at 30°C (0.030 mL g–1 h–1 O2, 0.021 mL g–1 h–1 CO2) than at 20°C (0.007 mL g–1 h–1 O2, 0.006 mL g–1 h–1 CO2) and the 20−30°C Q10 for O2 and CO2 were 4.60 and 3.55 respectively. Oxygen consumption rates at 15°C and 25°C were 0.002 (±0.000) and 0.018 (±0.000) mL g–1 h–1, with a corresponding Q10 of 9.21. Beyond ~30°C there was a decline in physiological performance, which was supported by activity patterns reported for P. umbrina in the literature.


2019 ◽  
Author(s):  
Dimitrios - Georgios Kontopoulos ◽  
Thomas P. Smith ◽  
Timothy G. Barraclough ◽  
Samraat Pawar

AbstractDeveloping 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—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 vs 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), two 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 two physiological rates underlying growth rate: net photosynthesis and respiration of plants. Furthermore, we find that these episodes of evolutionary convergence are consistent with two 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 where rapid evolution can occur at short time scales. Thus, more attention needs to be paid to elucidating the implications of rapid evolution in organismal thermal sensitivity for ecosystem functioning.Author summaryChanges in environmental temperature influence the performance of biological traits (e.g., respiration rate) in ectotherms, with the relationship between trait performance and temperature (the “thermal performance curve”) being single-peaked. Understanding how thermal performance curves adapt to different environments is important for predicting how organisms will be impacted by climate change. One key aspect of the shape of these curves is the thermal sensitivity near temperatures typically experienced by the species. Whether and how thermal sensitivity responds to different environments is a topic of active debate. To shed light on this, here we perform an evolutionary analysis of the thermal sensitivity of three key traits of prokaryotes, phytoplankton, and plants. We show that thermal sensitivity does not evolve in a gradual manner, but can differ considerably even between closely related species. This suggests that thermal sensitivity undergoes rapid adaptive evolution, which is further supported by our finding that thermal sensitivity varies weakly with latitude. We conclude that variation in thermal sensitivity arises partly from adaptation to environmental factors and that this may need to be accounted for in ecophysiological models.


Author(s):  
Hanna Scheuffele ◽  
Francesc Rubio-Gracia ◽  
Timothy D. Clark

Aerobic metabolic scope is a popular metric to estimate the capacity for temperature-dependent performance in aquatic animals. Despite this popularity, little is known of the role of temperature acclimation and variability in shaping the breadth and amplitude of the thermal performance curve for aerobic scope. If daily thermal experience can modify the characteristics of the thermal performance curve, interpretations of aerobic scope data from the literature may be misguided. Here, tropical barramundi (Lates calcarifer) were acclimated for ∼4 months to cold (23℃), optimal (29℃) or warm (35℃) conditions, or to a daily temperature cycle between 23 and 35℃ (with a mean of 29℃). Measurements of aerobic scope were conducted every 3-4 weeks at three temperatures (23℃, 29℃ and 35℃), and growth rates were monitored. Acclimation to constant temperatures caused some changes in aerobic scope at the three measurement temperatures via adjustments in standard and maximal metabolic rates, and growth rates were lower in the 23℃-acclimated group compared with all other groups. The metabolic parameters and growth rates of the thermally variable group remained similar to those of the 29℃-acclimated group. Thus, acclimation to a variable temperature regime did not broaden the thermal performance curve for aerobic scope. We propose that aerobic scope thermal performance curves are more plastic in amplitude rather than breadth, and that the metabolic phenotype of at least some fish may be more dependent on the mean daily temperature rather than on the daily temperature range.


2020 ◽  
Vol 223 (22) ◽  
pp. jeb233254
Author(s):  
Adriana P. Rebolledo ◽  
Carla M. Sgrò ◽  
Keyne Monro

ABSTRACTUnderstanding thermal performance at life stages that limit persistence is necessary to predict responses to climate change, especially for ectotherms whose fitness (survival and reproduction) depends on environmental temperature. Ectotherms often undergo stage-specific changes in size, complexity and duration that are predicted to modify thermal performance. Yet performance is mostly explored for adults, while performance at earlier stages that typically limit persistence remains poorly understood. Here, we experimentally isolate thermal performance curves at fertilization, embryo development and larval development stages in an aquatic ectotherm whose early planktonic stages (gametes, embryos and larvae) govern adult abundances and dynamics. Unlike previous studies based on short-term exposures, responses with unclear links to fitness or proxies in lieu of explicit curve descriptors (thermal optima, limits and breadth), we measured performance as successful completion of each stage after exposure throughout, and at temperatures that explicitly capture curve descriptors at all stages. Formal comparisons of descriptors using a combination of generalized linear mixed modelling and parametric bootstrapping reveal important differences among life stages. Thermal performance differs significantly from fertilization to embryo development (with thermal optimum declining by ∼2°C, thermal limits shifting inwards by ∼8–10°C and thermal breadth narrowing by ∼10°C), while performance declines independently of temperature thereafter. Our comparisons show that thermal performance at one life stage can misrepresent performance at others, and point to gains in complexity during embryogenesis, rather than subsequent gains in size or duration of exposure, as a key driver of thermal sensitivity in early life.


2019 ◽  
Author(s):  
Gregory W. Stegeman ◽  
Scott E. Baird ◽  
William S. Ryu ◽  
Asher D. Cutter

AbstractThermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its dynamic dependence on environmental stimuli presenting a challenge for analysis and for understanding the genomic architecture of heritable variation. Here we characterize behavioral reaction norms as thermal performance curves for the nematode Caenorhabditis briggsae, using a collection of 23 wild isolate genotypes and 153 recombinant inbred lines to quantify the extent of genetic and plastic variation in locomotory behavior to temperature changes. By reducing the dimensionality of the multivariate phenotypic response with a function-valued trait framework, we identified genetically distinct behavioral modules that contribute to the heritable variation in the emergent overall behavioral thermal performance curve. Quantitative trait locus mapping isolated regions on Chromosome II associated with locomotory activity at benign temperatures and Chromosome V loci related to distinct aspects of sensitivity to high temperatures, with each quantitative trait locus explaining up to 28% of trait variation. These findings highlight how behavioral responses to environmental inputs as thermal reaction norms can evolve through independent changes to genetically distinct modular components of such complex phenotypes.Article SummaryPlastic responses to environmental inputs, reaction norm phenotypes that can be summarized with parameters of fits to a mathematical function, are pervasive across diverse organismal traits and crucial to organismal fitness. We quantified the nematode Caenorhabditis briggsae’s behavioral thermal performance curves as function-valued traits for 23 wild isolate genotypes and 153 recombinant inbred lines. We identified quantitative trait loci on multiple chromosomes that define genetically distinct behavioral modules contributing to the emergent overall behavioral thermal performance curve. These findings highlight how dynamic behavioral responses to environmental inputs can evolve through independent changes to genetically distinct modular components of such complex phenotypes.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hsiang-Yu Tsai ◽  
Dustin R Rubenstein ◽  
Bo-Fei Chen ◽  
Mark Liu ◽  
Shih-Fan Chan ◽  
...  

Understanding how climate-mediated biotic interactions shape thermal niche width is critical in an era of global change. Yet, most previous work on thermal niches has ignored detailed mechanistic information about the relationship between temperature and organismal performance, which can be described by a thermal performance curve. Here, we develop a model that predicts the width of thermal performance curves will be narrower in the presence of interspecific competitors, causing a species’ optimal breeding temperature to diverge from that of its competitor. We test this prediction in the Asian burying beetle Nicrophorus nepalensis, confirming that the divergence in actual and optimal breeding temperatures is the result of competition with their primary competitor, blowflies. However, we further show that intraspecific cooperation enables beetles to outcompete blowflies by recovering their optimal breeding temperature. Ultimately, linking abiotic factors and biotic interactions on niche width will be critical for understanding species-specific responses to climate change.


2019 ◽  
Vol 112 (4) ◽  
pp. 1560-1574 ◽  
Author(s):  
Kelsey A McCalla ◽  
Mehmet Keçeci ◽  
Ivan Milosavljević ◽  
David A Ratkowsky ◽  
Mark S Hoddle

AbstractThis study examined the effects of seven constant and fluctuating temperature profiles with corresponding averages of 12 to 38°C on the life history of the Punjab, Pakistan-sourced Tamarixia radiata (Waterston) released in California for biological control of Diaphorina citri Kuwayama. One linear and seven nonlinear regression functions were fit to egg-to-adult development rate data to characterize thermal performance curves. Temperature fluctuations significantly affected both development and longevity of T. radiata. Estimates of degree-days predicted by the linear model were 30% higher for the fluctuating regime than the constant regime. Nonlinear model estimations of theoretical minimum and maximum developmental thresholds were lower for the fluctuating regime when compared to the constant regime. These predictions align with experimental observations. Parasitoids reared under fluctuating profiles at low average temperatures developed faster (15°C) and survived longer (15–20°C) when compared to those reared under constant regimes with corresponding means. In contrast, high average fluctuating temperatures produced parasitoids with an extended developmental period (35°C) and reduced longevity (30–35°C). A meta-analysis of published T. radiata development datasets, together with the results of this study, indicated convergence in degree-days and theoretical minimum developmental thresholds among geographically distinct parasitoid populations. These findings demonstrate the significant effects of temperature on T. radiata life history and have important implications for optimization of mass-rearing and release efforts, improvement of predictions from climate modeling, and comparison of T. radiata population performance across climatic gradients and geographic regions.


Author(s):  
María Aranguren-Gassis ◽  
Elena Litchman

Abstract Environmental factors that interact with increasing temperature under the ongoing global warming are an urgent issue determining marine phytoplankton’s performance. Previous studies showed that nutrient limitation alters phytoplankton responses to temperature and may lower their temperature optima (Topt), making them more susceptible to high temperatures. The generality of this relationship is unknown, as very few species were tested. Here we investigated how growth rate depended on temperature at two contrasting nitrogen concentrations in six marine diatoms isolated from different thermal environments, including the tropics. Low nitrate had a significant effect on thermal performance in five of the six species. The effect size was larger around the optimum temperature for growth, resulting in flattened thermal performance curves but no shift in Topt. While that trend is independent of the thermal regime from which each species was isolated, the implications for the phytoplankton response to global warming may be region dependent.


2018 ◽  
Vol 285 (1878) ◽  
pp. 20180697 ◽  
Author(s):  
Michael L. Logan ◽  
John David Curlis ◽  
Anthony L. Gilbert ◽  
Donald B. Miles ◽  
Albert K. Chung ◽  
...  

Ectothermic species are particularly sensitive to changes in temperature and may adapt to changes in thermal environments through evolutionary shifts in thermal physiology or thermoregulatory behaviour. Nevertheless, the heritability of thermal traits, which sets a limit on evolutionary potential, remains largely unexplored. In this study, we captured brown anole lizards ( Anolis sagrei ) from two populations that occur in contrasting thermal environments. We raised offspring from these populations in a laboratory common garden and compared the shape of their thermal performance curves to test for genetic divergence in thermal physiology. Thermal performance curves differed between populations in a common garden in ways partially consistent with divergent patterns of natural selection experienced by the source populations, implying that they had evolved in response to selection. Next, we estimated the heritability of thermal performance curves and of several traits related to thermoregulatory behaviour. We did not detect significant heritability in most components of the thermal performance curve or in several aspects of thermoregulatory behaviour, suggesting that contemporary selection is unlikely to result in rapid evolution. Our results indicate that the response to selection may be slow in the brown anole and that evolutionary change is unlikely to keep pace with current rates of environmental change.


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