Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour

2002 ◽  
Vol 205 (15) ◽  
pp. 2305-2322 ◽  
Author(s):  
Ian A. Johnston ◽  
Genevieve K. Temple

SUMMARY Seasonal cooling can modify the thermal preferenda of ectothermic vertebrates and elicit a variety of physiological responses ranging from winter dormancy to an acclimation response that partially compensates for the effects of low temperature on activity. Partial compensation of activity levels is particularly common in aquatic species for which seasonal temperature changes provide a stable cue for initiating the response. Thermal plasticity of locomotory performance has evolved independently on numerous occasions, and there is considerable phylogenetic diversity with respect to the mechanisms at the physiological and molecular levels. In teleosts,neuromuscular variables that can be modified include the duration of motor nerve stimulation, muscle activation and relaxation times, maximum force and unloaded shortening velocity (Vmax), although not all are modified in every species. Thermal plasticity in Vmax has been associated with changes in myosin ATPase activity and myosin heavy chain(MyHC) composition and/or with a change in the ratio of myosin light chain isoforms. In common carp (Cyprinus carpio), there are continuous changes in phenotype with acclimation temperature at lower levels of organisation, such as MyHC composition and Vmax, but a distinct threshold for an effect in terms of locomotory performance. Thus,there is no simple relationship between whole-animal performance and muscle phenotype. The nature and magnitude of temperature acclimation responses also vary during ontogeny. For example, common carp acquire the ability to modify MyHC composition with changes in acclimation temperature during the juvenile stage. In contrast, the thermal plasticity of swimming performance observed in tadpoles of the frog Limnodynastes peronii is lost in the terrestrial adult stage. Although it is often assumed that the adjustments in locomotory performance associated with temperature acclimation enhance fitness, this has rarely been tested experimentally. Truly integrative studies of temperature acclimation are scarce, and few studies have considered both sensory and motor function in evaluating behavioural responses. Developmental plasticity is a special case of a temperature acclimation response that can lead to temporary or permanent changes in morphology and/or physiological characteristics that affect locomotory performance.

2021 ◽  
Vol 8 (7) ◽  
pp. 210440
Author(s):  
Melissa K. Drown ◽  
Amanda N. DeLiberto ◽  
Moritz A. Ehrlich ◽  
Douglas L. Crawford ◽  
Marjorie F. Oleksiak

To better understand temperature's role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus (small estuarine fish) populations from different thermal environments. Fundulus heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographical cline. In this study, we use three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ, and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12 or 28°C, we quantified whole-animal metabolic (WAM) rate, critical thermal maximum (CT max ) and substrate-specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous (i.e. no added substrates)) in approximately 160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within populations. In general, for WAM and CT max , the interindividual variation in acclimation response (log 2 ratio 28/12°C) was a function of performance at 12°C and order of acclimation (12–28°C versus 28–12°C). CT max and WAM were greater at 28°C than 12°C, although WAM had a small change (2.32-fold) compared with the expectation for a 16°C increase in temperature (expect 3- to 4.4-fold). By contrast, for CaM, the rates when acclimatized and assayed at 12 or 28°C were nearly identical. The small differences in CaM between 12 and 28°C temperature were partially explained by cardiac remodeling where individuals acclimatized to 12°C had larger hearts than individuals acclimatized to 28°C. Correlation among physiological traits was dependent on acclimation temperature. For example, WAM was negatively correlated with CT max at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher CaM than fatty acid, and fatty acid supported higher CaM than lactate, ketones and alcohol (LKA) or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These findings suggest interindividual variation in physiological responses to temperature acclimation and indicate that additional research investigating interindividual may be relevant for global climate change responses in many species.


1981 ◽  
Vol 240 (1) ◽  
pp. R93-R98 ◽  
Author(s):  
P. S. Rutledge

Crayfish, Pacifastacus leniusculus, were acclimated to 10, 20, and 25 degrees C for 1 mo. Hemocyanin from animals at these three acclimation temperatures showed distinctly different oxygen binding patterns. At any particular set of test temperature and pH, hemocyanin from 10 degrees C-acclimated animals had the lowest oxygen affinity and the greatest cooperativity, whereas hemocyanin from 25 degrees C-acclimated animals had the highest oxygen affinity and the lowest cooperativity. When tested at their own acclimation temperature, and at normal hemolymph pH for that temperature, all three hemocyanins showed oxygen pressure for half-saturation of hemoglobin of 6-7 Torr. Thus acclimation keeps oxygen affinity centered around a narrow range of values. The acclimation response probably eliminates hemocyanin oxygen affinity as a major factor in the decline of oxygen uptake ability in the crayfish above 20 degrees C. The structural basis for the observed functional changes in the hemocyanin is not yet clear.


2000 ◽  
Vol 279 (2) ◽  
pp. R657-R665 ◽  
Author(s):  
James M. Wakeling ◽  
Nicholas J. Cole ◽  
Kirsty M. Kemp ◽  
Ian A. Johnston

The effects of thermal acclimation were investigated in the common carp Cyprinus carpio L. Acclimation and acute temperature effects were tested during ontogeny from larval [9.5 mm total length ( L)] to juvenile (69.0 mm L) stages and between 8 and 21°C. The myosin heavy chain (MHC) composition, myofibrillar Mg2+-Ca2+-ATPase activity, and muscle strains showed significant thermal acclimation effects. MHCs were only expressed in an acclimation temperature-dependent fashion in fish longer than 37 mm. During fast starts, the temperature had a significant effect on the white muscle strain (33% increase and 50% decrease with increasing acclimation and acute temperature, respectively) and contraction duration (25% decrease with increasing acute temperature). Increases in hydrodynamic efficiency (0.19 to 0.38) and hydrodynamic power requirements (Q10 = 3.2) occurred with increasing acute temperature (10 to 20 °C). Competing hypotheses about the evolutionary significance of the temperature acclimation response were tested. Acclimation extended the temperature range for fast-start behavior, but no improvements in performance at the whole animal level were found between 8 and 21°C.


BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Isabella Loughland ◽  
Alexander Little ◽  
Frank Seebacher

Abstract Background Thermal plasticity is pivotal for evolution in changing climates and in mediating resilience to its potentially negative effects. The efficacy to respond to environmental change depends on underlying mechanisms. DNA methylation induced by DNA methyltransferase 3 enzymes in the germline or during early embryonic development may be correlated with responses to environmental change. This developmental plasticity can interact with reversible acclimation within adult organisms, which would increase the speed of response and could alleviate potential mismatches between parental or early embryonic environments and those experienced at later life stages. Our aim was to determine whether there is a causative relationship between DNMT3 enzyme and developmental thermal plasticity and whether either or both interact with short-term acclimation to alter fitness and thermal responses in zebrafish (Danio rerio). Results We developed a novel DNMT3a knock-out model to show that sequential knock-out of DNA methyltransferase 3a isoforms (DNMT3aa−/− and DNMT3aa−/−ab−/−) additively decreased survival and increased deformities when cold developmental temperatures in zebrafish offspring mismatched warm temperatures experienced by parents. Interestingly, short-term cold acclimation of parents before breeding rescued DNMT3a knock-out offspring by restoring survival at cold temperatures. DNMT3a knock-out genotype interacted with developmental temperatures to modify thermal performance curves in offspring, where at least one DNMT3a isoform was necessary to buffer locomotion from increasing temperatures. The thermal sensitivity of citrate synthase activity, an indicator of mitochondrial density, was less severely affected by DNMT3a knock-out, but there was nonetheless a significant interaction between genotype and developmental temperatures. Conclusions Our results show that DNMT3a regulates developmental thermal plasticity and that the phenotypic effects of different DNMT3a isoforms are additive. However, DNMT3a interacts with other mechanisms, such as histone (de)acetylation, induced during short-term acclimation to buffer phenotypes from environmental change. Interactions between these mechanisms make phenotypic compensation for climate change more efficient and make it less likely that thermal plasticity incurs a cost resulting from environmental mismatches.


2021 ◽  
Author(s):  
Angela Carolina Guillen ◽  
Marcelo Eduardo Borges ◽  
Tatiana Herrerias ◽  
Priscila Krebsbach Kandalski ◽  
Maria Rosa Dmengeon Pedreiro de Souza ◽  
...  

Abstract Antarctica is considered a thermally stable ecosystem; however, climate studies point to increases in air and surface water temperatures in this region. These thermal changes may affect the biological processes of animals inhabiting such regions because they are stress factors and may promote metabolic changes, rendering the animals more vulnerable to oxidative damage. Plasma parameters are also good indicators of stress and allow analysis of the metabolic status of fish under temperature increases. The present study assessed the effect of acclimation temperature on the levels of plasma, osmoregulatory and oxidative metabolism parameters and antioxidant defenses in kidney, gill, liver and brain tissues of Notothenia rossii subjected to gradual temperature changes of 0.5°C/day until reaching temperatures of 2, 4, 6 and 8°C. Under the effect of the 0.5°C/day acclimation rate, gill tissue showed increased glutathione-S-transferase (GST) activity, and kidney tissue showed increased H⁺-ATPase at 9 days of the experiment (2°C). In the liver, consistent increases in the MDA concentration as an indicator of lipid peroxidation (9 (2°C),13 (4°C),17 (6°C) and 21 (6°C) days) were noted, as well as an increase in GSH at 9 days (2°C). In plasma, gradual decreases in the concentrations of total proteins and globulins were observed. These responses indicate the presence of thermal plasticity and an attempt at regulation to mitigate thermal stress. The changes showed that a gradual increase in temperature may cause opposite responses to the thermal shock model in N. rossii.


1990 ◽  
Vol 259 (2) ◽  
pp. R231-R236 ◽  
Author(s):  
I. A. Johnston ◽  
J. D. Fleming ◽  
T. Crockford

After several weeks of cold acclimation, the swimming performance of some fish is increased at low temperatures and decreased at high temperatures. The temperature compensation of locomotory activity involves changes in central patterns of muscle fiber recruitment and in the properties of the peripheral nervous system and muscle tissues. In some freshwater fish belonging to the family Cyprinidae, including the goldfish (Carassius auratus), the common carp (Cyprinus carpio), and the roach (Rutilus rutilus), the intrinsic contractile properties of muscles are modified by thermal acclimation. Parameters that can be altered by temperature acclimation in both fast and slow muscle fibers include isometric twitch contraction time, maximum force production, and unloaded shortening speed. The molecular mechanisms responsible for these changes in contractility are discussed.


2001 ◽  
Vol 204 (1) ◽  
pp. 39-45 ◽  
Author(s):  
F.B. Jensen ◽  
T. Wang ◽  
J. Brahm

Unidirectional (36)Cl(−) efflux via the red blood cell anion exchanger was measured under Cl(−) self-exchange conditions (i.e. no net flow of anions) in rainbow trout Oncorhynchus mykiss and red-eared freshwater turtle Trachemys scripta to examine the effects of acute temperature changes and acclimation temperature on this process. We also evaluated the possible adaptation of anion exchange to different temperature regimes by including our previously published data on other animals. An acute temperature increase caused a significant increase in the rate constant (k) for unidirectional Cl(−) efflux in rainbow trout and freshwater turtle. After 3 weeks of temperature acclimation, 5 degrees C-acclimated rainbow trout showed only marginally higher Cl(−) transport rates than 15 degrees C-acclimated trout when compared at the same temperature. Apparent activation energies for red blood cell Cl(−) exchange in trout and turtle were lower than values reported in endothermic animals. The Q(10) for red blood cell anion exchange was 2.0 in trout and 2.3 in turtle, values close to those for CO(2) excretion, suggesting that, in ectothermic animals, the temperature sensitivity of band-3-mediated anion exchange matches the temperature sensitivity of CO(2) transport (where red blood cell Cl(−)/HCO(3)(−) exchange is a rate-limiting step). In endotherms, such as man and chicken, Q(10) values for red blood cell anion exchange are considerably higher but are no obstacle to CO(2) transport, because body temperature is normally kept constant at values at which anion exchange rates are high. When compared at constant temperature, red blood cell Cl(−) permeability shows large differences among species (trout, carp, eel, cod, turtle, alligator, chicken and man). Cl(−) permeabilities are, however, remarkable similar when compared at preferred body temperatures, suggesting an appropriate evolutionary adaptation of red blood cell anion exchange function to the different thermal niches occupied by animals.


1994 ◽  
Vol 267 (4) ◽  
pp. R1150-R1153 ◽  
Author(s):  
J. A. Segal ◽  
D. L. Crawford

The temperature-dependent expression of lactate dehydrogenase-B (LDH-B) was compared between two environmentally distinct populations of Fundulus heteroclitus acclimated to 10 degrees C and 20 degrees C. The variability in LDH-B protein expression both within and between populations is consistent with a model of thermal compensation. The northern population from the colder environment expresses a twofold greater amount of LDH-B protein than the warmer southern population at both acclimation temperatures. Correspondingly, both populations have 1.3-fold greater levels of the enzyme at an acclimation temperature of 10 degrees C in comparison to 20 degrees C. In 20 degrees C-acclimated individuals there is a similar twofold difference between populations for LDH-B mRNA concentrations, and LDH-B protein and mRNA are highly correlated (r = 0.81). After acclimation to 10 degrees C, this difference between populations is not seen and in the northern population there is no relationship between LDH-B mRNA and protein levels. Thus the molecular mechanism regulating LDH-B enzyme expression changes in response to temperature acclimation and is different between populations.


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