Publications by authors named "Jeffrey G Richards"

59 Publications

Behavioural variation between piscivore and insectivore rainbow trout Oncorhynchus mykiss.

J Fish Biol 2021 May 10. Epub 2021 May 10.

Department of Zoology, The University of British Columbia, Vancouver, British Columbia, Canada.

A proactive-reactive continuum integrating multiple (i.e., 3+) dimensions of animal behaviour has been reported as a major axis of behavioural differentiation, but its stability along a biological hierarchy from individuals to populations remains speculative. Piscivore and insectivore rainbow trout (Oncorhynchus mykiss) represent closely related ecotypes with strong ecological divergence driven by selection for a large-bodied piscivorous lifestyle with fast juvenile growth vs. selection for smaller adult body size and lower growth associated with an insectivorous diet. To evaluate whether differences in behaviour between ecotypes are consistent with a proactive-reactive axis and consistent along a biological hierarchy, the authors examined variation in emergence time from a shelter, exploration, activity and predator inspection among individuals, populations and ecotypes of juvenile piscivore and insectivore rainbow trout O. mykiss. As expected, the faster-growing piscivore ecotype was more proactive (i.e., shorter emergence time, exploration and predator inspection) than the more reactive insectivore ecotype. This behavioural contrast was partly maintained across populations, although activity differences were most pronounced among populations, rather than emergence time. Insectivore fry showed substantial variation in behavioural expression among individuals within populations; by contrast, piscivores showed highly similar proactive behaviours with significantly lower inter-individual variation in behavioural expression, suggesting intense selection on behaviour supporting their faster growth. This work suggests that piscivore and insectivore O. mykiss broadly differ in behaviour along a proactive vs. reactive continuum, and highlights the greater multidimensionality of behavioural expression within the insectivore ecotype. Contrasting behaviours between ecotypes may result from differential selection for slow vs. fast juvenile growth and associated metabolism, and may contribute to adult trophic specialization.
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http://dx.doi.org/10.1111/jfb.14781DOI Listing
May 2021

Adaptive differentiation of growth, energetics and behaviour between piscivore and insectivore juvenile rainbow trout along the Pace-of-Life continuum.

J Anim Ecol 2020 11 12;89(11):2717-2732. Epub 2020 Oct 12.

Department of Zoology, The University of British Columbia, Vancouver, BC, Canada.

Adaptive trade-offs are fundamental mechanisms underlying phenotypic diversity, but the presence of generalizable patterns in multivariate adaptation and their mapping onto environmental gradients remain unclear. To understand how life history affects multivariate trait associations, we examined relationships among growth, metabolism, anatomy and behaviour in rainbow trout juveniles from piscivore versus insectivore ecotypes along an experimental gradient of food availability. We hypothesized that (a) selection for larger size in piscivorous adults would select for higher juvenile growth at the cost of lower active metabolism; (b) elevated growth of piscivores would be supported by a greater productivity of their natal stream and more proactive foraging behaviours and (c) general patterns of multivariate trait associations would match the predictions of the Pace-Of-Life Syndrome. Relative to insectivores, piscivorous fry showed a pattern of higher growth (+63%), maximum food intake (+33%), growth efficiency (+41%) and standard metabolic rate (SMR; +47%), but lower active metabolic capacity (maximum metabolic rate [MMR; -17%], aerobic scope [AS; -48%]), suggesting that faster piscivore growth is supported by greater food intake and digestive capacity but is traded-off against lower scope for active metabolism. A similar trade-off appeared among organ systems, with piscivorous fry exhibiting an 83% greater investment in average mass of organs associated with food consumption and processing (i.e. stomach and intestine), but an apparently smaller relative investment in organs involved in cardiovascular or cognitive activities (heart and brain, respectively). Higher invertebrate drift in their natal rearing habitat, quicker behavioural transition to a novel food source and lower anxiety after a frightening event in piscivorous fry suggest that faster growth requires both proactive foraging behaviours and higher prey availability in the environment. Finally, the sampling of replicate insectivore populations confirmed their lower juvenile growth (-73% on average) and reduced environmental productivity of their natal streams (-45% lower drift abundance) relative to the piscivore ecotype. Our results suggest that selection for large adult body size influences selection on high juvenile growth, high basal metabolism and proactive behaviours, and that the intense phenotypic divergence between piscivorous and insectivorous rainbow trout may be constrained by environmental productivity.
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http://dx.doi.org/10.1111/1365-2656.13326DOI Listing
November 2020

Reduced hypoxia tolerance and survival at elevated temperatures may limit the ability of Amazonian fishes to survive in a warming world.

Sci Total Environ 2020 Dec 2;748:141349. Epub 2020 Aug 2.

Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada. Electronic address:

The Amazon basin contains more than 20% of the world's freshwater fishes, many of ecological and economical importance. An increase in temperature of 2.2 to 7 °C is predicted to occur within the next century in the worst-case scenario of climate change predictions, which will likely be associated with an increase in the prevalence and duration of reduced water oxygen levels (hypoxia). Furthermore, there is an increasing frequency of heat waves in the Amazon basin, which exacerbates issues related to temperature and hypoxia. Increases in temperature and hypoxia both constrain an organism's ability to supply oxygen to metabolizing tissues, thus the ability to cope with thermal and hypoxic stress may be correlated. Here, we reveal a positive correlation between acute thermal tolerance and acute hypoxia tolerance amongst 37 Amazonian fish species at the current river temperatures of 28-31 °C. The effects of long-term (10 days or 4 weeks) increases in temperature were investigated in a subset of 13 species and demonstrated that 2 species failed to acclimate and survive at 33 °C, 9 species failed at 35 °C, and only 2 species survived up to 35 °C. Of those that survived long-term exposure to 33 or 35 °C, the majority of the species demonstrated only an improvement in acute thermal tolerance. In contrast, hypoxia tolerance was reduced following acute- and long-term exposure to 33, 35 or 37 °C in all species investigated. The results of this study suggest that many of the fish species that inhabit the Amazon may be at risk during both short- and long-term temperature increases and these risks are exacerbated by the associated environmental hypoxia.
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http://dx.doi.org/10.1016/j.scitotenv.2020.141349DOI Listing
December 2020

Interactive effects of temperature and hypoxia on diffusive water flux and oxygen uptake rate in the tidepool sculpin, Oligocottus maculosus.

Comp Biochem Physiol A Mol Integr Physiol 2020 12 5;250:110781. Epub 2020 Aug 5.

Department of Zoology, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada.

The osmorespiratory compromise hypothesis posits that respiratory epithelial characteristics and physiological regulatory mechanisms which promote gas permeability also increase permeability to ions and water. The hypothesis therefore predicts that physiological responses which increase effective gas permeability will result in increased effective ion and water permeabilities. Though analyses of water and gas effective permeabilities using high temperature have generally supported the hypothesis, water permeability responses to hypoxia remain equivocal and the combination of high temperature and hypoxia untested. We measured diffusive water flux (DWF) and oxygen uptake rate (Ṁo) in response to acute temperature change, hypoxia, and the combination of high temperature and hypoxia in a hypoxia-tolerant intertidal fish, the tidepool sculpin (Oligocottus maculosus). In support of the osmorespiratory compromise hypothesis, Ṁo and DWF increased with temperature. In contrast, DWF decreased with hypoxia at a constant temperature, a result consistent with previously observed decoupling of water and gas effective permeabilities during hypoxia exposure in some hypoxia tolerant fishes. However, DWF levels during simultaneous high temperature and hypoxia exposure were not different from fish exposed to high temperature in normoxia, possibly suggesting a failure of the mechanism responsible for down-regulating DWF in hypoxia. These results, together with time-course analysis of hypoxia exposure and normoxic recovery, suggest that tidepool sculpins actively downregulate effective water permeability in hypoxia but the mechanism fails with multi-stressor exposure. Future investigations of the mechanistic basis of the regulation of gill permeability will be key to understanding the role of this regulatory ability in the persistence of this species in the dynamic intertidal environment.
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http://dx.doi.org/10.1016/j.cbpa.2020.110781DOI Listing
December 2020

Species- and tissue-specific differences in ROS metabolism during exposure to hypoxia and hyperoxia plus recovery in marine sculpins.

J Exp Biol 2019 11 21;222(Pt 22). Epub 2019 Nov 21.

Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, BC V6T 1Z4, Canada.

Animals that inhabit environments that fluctuate in oxygen must not only contend with disruptions to aerobic metabolism, but also the potential effects of reactive oxygen species (ROS). The goal of this study was to compare aspects of ROS metabolism in response to O variability (6 h hypoxia or hyperoxia, with subsequent normoxic recovery) in two species of intertidal sculpin fishes (Cottidae, Actinopterygii) that can experience O fluctuations in their natural environment and differ in whole-animal hypoxia tolerance. To assess ROS metabolism, we measured the ratio of glutathione to glutathione disulfide as an indicator of tissue redox environment, MitoP/MitoB ratio to assess mitochondrial ROS generation, thiobarbituric acid reactive substances (TBARS) for lipid peroxidation, and total oxidative scavenging capacity (TOSC) in the liver, brain and gill. In the brain, the more hypoxia-tolerant showed large increases in TBARS levels following hypoxia and hyperoxia exposure that were generally not associated with large changes in mitochondrial HO In contrast, the less-tolerant showed no significant changes in TBARS or mitochondrial HO in the brain. More moderate increases were observed in the liver and gill of exposed to hypoxia and hyperoxia with normoxic recovery, whereas had a greater response to O variability in these tissues compared with the brain. Our results show a species- and tissue-specific relationship between hypoxia tolerance and ROS metabolism.
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http://dx.doi.org/10.1242/jeb.206896DOI Listing
November 2019

Detection of changes in mitochondrial hydrogen sulfide in the fish model (Poeciliidae).

Biol Open 2019 May 9;8(5). Epub 2019 May 9.

MRC Mitochondrial Biology Unit, University of Cambridge, Hills Road, Cambridge CB2 0XY, UK

In this paper, we outline the use of a mitochondria-targeted ratiometric mass spectrometry probe, MitoA, to detect changes in mitochondrial hydrogen sulfide (HS) in (family Poeciliidae). MitoA is introduced via intraperitoneal injection into the animal and is taken up by mitochondria, where it reacts with HS to form the product MitoN. The MitoN/MitoA ratio can be used to assess relative changes in the amounts of mitochondrial HS produced over time. We describe the use of MitoA in the fish species to illustrate the steps for adopting the use of MitoA in a new organism, including extraction and purification of MitoA and MitoN from tissues followed by tandem mass spectrometry. In this proof-of-concept study we exposed HS tolerant to 59 µM free HS for 5 h, which resulted in increased MitoN/MitoA in brain and gills, but not in liver or muscle, demonstrating increased mitochondrial HS levels in select tissues following whole-animal HS exposure. This is the first time that accumulation of HS has been observed during whole-animal exposure to free HS using MitoA. This article has an associated First Person interview with the first author of the paper.
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http://dx.doi.org/10.1242/bio.041467DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6550084PMC
May 2019

Don't throw the fish out with the respirometry water.

J Exp Biol 2019 03 28;222(Pt 6). Epub 2019 Mar 28.

Department of Zoology, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4.

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http://dx.doi.org/10.1242/jeb.200253DOI Listing
March 2019

The effects of salinity and photoperiod on aerobic scope, hypoxia tolerance and swimming performance of coho salmon (Oncorhynchus kisutch) reared in recirculating aquaculture systems.

Comp Biochem Physiol A Mol Integr Physiol 2019 05 4;231:82-90. Epub 2019 Feb 4.

Department of Zoology, The University of British Columbia, 6270 University Blvd., Vancouver, BC V6T 1Z4, Canada. Electronic address:

Land-based recirculating aquaculture systems (RAS) have been used to rear salmon from smolt to market-sized adults, but high operating costs have limited their wide spread adoption. One clear advantage of using RAS for salmon aquaculture over open net pens is that fish can be reared under optimal conditions in an attempt to maximize growth and physiological performance and reduce overall production costs. However, few studies have attempted to define the optimal conditions for the long-term rearing of salmon. Thus, the goal of this study is to determine the effects of salinity and photoperiod, two factors that can be easily manipulated in RAS, on the physiological performance of coho salmon (Oncorhynchus kisutch) during long-term rearing. To address this goal, post-smolt coho salmon were reared for 150 days in replicate RAS at 2.5, 5, 10 and 30 ppt under either 12:12 and 24:0 (light:dark) photoperiods. Routine metabolic rate, maximum metabolic rate, aerobic scope and hypoxia tolerance were measured at 60 and 120 days of rearing, while swimming performance was assessed at 60 and 150 days of rearing. There were no effects of salinity or photoperiod on metabolic rate measurements, hypoxia tolerance or swimming performance at any sampling time. There were, however, significant effects of salinity and photoperiod on post-swimming hematology. The results suggest that physiological disturbances continue to manifest due to different environmental conditions, despite acclimation, but do not hinder the animal's ability to cope with physiological stressors. Overall, rearing salinity and photoperiod had very few measurable effects on the physiology and performance of coho salmon except the ionoregulatory disturbances following swimming at salinities of 2.5 and 30 ppt.
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http://dx.doi.org/10.1016/j.cbpa.2019.01.026DOI Listing
May 2019

The effect of salinity and photoperiod on thermal tolerance of Atlantic and coho salmon reared from smolt to adult in recirculating aquaculture systems.

Comp Biochem Physiol A Mol Integr Physiol 2019 04 24;230:1-6. Epub 2018 Dec 24.

Department of Zoology, The University of British Columbia, 6270 University Blvd., Vancouver, BC V6T 1Z4, Canada.

Land-based, closed containment salmon aquaculture involves rearing salmon from smolt to adult in recirculating aquaculture systems (RAS). Unlike in open-net pen aquaculture, rearing conditions can be specified in RAS in order to optimize growth and physiological stress tolerance. The environmental conditions that yield optimal stress tolerance in salmon are, however, unknown. To address this knowledge gap, we reared Atlantic (Salmo salar) and coho (Oncorhynchus kisutch) salmon in 7 separate RASs for 400 days post-smoltification under 2 photoperiods (24:0 or 12:12, light:dark) and 4 salinities (2.5, 5, 10 or 30 ppt.) and assessed the effects of these conditions on thermal tolerance. We found that over the first 120 days post-smoltification, rearing coho under a 24:0 photoperiod resulted in a ~2 °C lower critical thermal maxima (CT) than in coho reared under a 12:12 photoperiod. This photoperiod effect did not persist at 200 and 400 days, which was coincident with an overall decrease in CTmax in coho. Finally, Atlantic salmon had a higher CT (~28 °C) compared to coho (~26 °C) at 400 days post-smoltification. Overall, these findings are important for the future implications of RAS and for the aquaculture industry to help identify physiologically sensitive time stages.
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http://dx.doi.org/10.1016/j.cbpa.2018.12.008DOI Listing
April 2019

Effects of cold on murine brain mitochondrial function.

PLoS One 2018 6;13(12):e0208453. Epub 2018 Dec 6.

Department of Zoology, University of British Columbia, Vancouver, British Columbia, CAN.

Therapeutic hypothermia is a strategy that reduces metabolic rate and brain damage during clinically-relevant hypoxic events. Mitochondrial respiration is compromised by hypoxia, with deleterious consequences for the mammalian brain; however, little is known about the effects of reduced temperature on mitochondrial metabolism. Therefore, we examined how mitochondrial function is impacted by temperature using high resolution respirometry to assess electron transport system (ETS) function in saponin-permeabilized mouse brain at 28 and 37°C. Respirometric analysis revealed that, at the colder temperature, ETS respiratory flux was ~ 40-75% lower relative to the physiological temperature in all respiratory states and for all fuel substrates tested. In whole brain tissue, the enzyme maximum respiratory rates for complexes I-V were similarly reduced by between 37-88%. Complexes II and V were particularly temperature-sensitive; a temperature-mediated decrease in complex II activity may support a switch to complex I mediated ATP-production, which is considerably more oxygen-efficient. Finally, the mitochondrial H+-gradient was more tightly coupled, indicating that mitochondrial respiration is more efficient at the colder temperature. Taken together, our results suggest that improvements in mitochondrial function with colder temperatures may contribute to energy conservation and enhance cellular viability in hypoxic brain.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0208453PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6283463PMC
May 2019

Interspecific variation in brain mitochondrial complex I and II capacity and ROS emission in marine sculpins.

J Exp Biol 2019 01 28;222(Pt 2). Epub 2019 Jan 28.

Department of Zoology, The University of British Columbia, 6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4.

Environmental hypoxia presents a metabolic challenge for animals because it inhibits mitochondrial respiration and can lead to the generation of reactive oxygen species (ROS). We investigated the interplay between O use for aerobic respiration and ROS generation among sculpin fishes (Cottidae, Actinopterygii) that are known to vary in whole-animal hypoxia tolerance. We hypothesized that mitochondria from hypoxia-tolerant sculpins would show more efficient O use with a higher phosphorylation efficiency and lower ROS emission. We showed that brain mitochondria from more hypoxia-tolerant sculpins had lower complex I and higher complex II flux capacities compared with less hypoxia-tolerant sculpins, but these differences were not related to variation in phosphorylation efficiency (ADP/O) or mitochondrial coupling (respiratory control ratio). The hypoxia-tolerant sculpins had higher mitochondrial HO emission per O consumed (HO/O) under oligomycin-induced state 4 conditions compared with less hypoxia-tolerant sculpins. An redox challenge experiment revealed species differences in how well mitochondria defend their glutathione redox status when challenged with high levels of reduced glutathione, but the redox challenge elicited the same HO/O in all species. Furthermore, anoxia recovery lowered absolute HO emission (HO per mg mitochondrial protein) in all species and negatively impacted state 3 respiration rates in some species, but the responses were not related to hypoxia tolerance. Overall, we clearly demonstrate a relationship between hypoxia tolerance and complex I and II flux capacities in sculpins, but the differences in complex flux capacity do not appear to be directly related to variation in ROS metabolism.
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http://dx.doi.org/10.1242/jeb.189407DOI Listing
January 2019

Variable gene transcription underlies phenotypic convergence of hypoxia tolerance in sculpins.

BMC Evol Biol 2018 11 3;18(1):163. Epub 2018 Nov 3.

Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, BC, V6T 1Z4, Canada.

Background: The degree by which mechanisms underlying phenotypic convergence are similar among taxa depends on the number of evolutionary paths available for selection to act upon. Likelihood of convergence will be influenced by an interplay of factors such as genetic architecture, phylogenetic history and population demography. To determine if there is convergence or divergence in mechanisms underlying phenotypic similarity, we assessed whether gene transcription patterns differed among species with similar levels of hypoxia tolerance.

Results: Three species of marine fish from the superfamily Cottoidea (smoothhead sculpin [Artedius lateralis], sailfin sculpin [Nautichthys oculofasciatus] and Pacific staghorn sculpin [Leptocottus armatus]), all of which have previously been shown to share the same level of hypoxia tolerance, were exposed to short-(8 h) and longer-term (72 h) hypoxia and mRNA transcripts were assessed using a custom microarray. We examined hypoxia-induced transcription patterns in metabolic and protein production pathways and found that a high proportion of genes associated with these biological processes showed significant differences among the species. Specifically, the data suggest that the smoothhead sculpin, unlike the sailfin sculpin and the Pacific staghorn sculpin, relied on amino acid degradation rather than glycolysis or fatty acid oxidation to generate ATP during hypoxia exposure. There was also variation across the species in the transcription of genes involved in protein production (e.g. mRNA processing and protein translation), such that it increased in the smoothhead sculpin, decreased in the sailfin sculpin and was variable in the Pacific staghorn sculpin.

Conclusions: Changes in metabolic and protein production pathways are part of the key responses of fishes to exposures to environmental hypoxia. Yet, species with similar overall hypoxia tolerance exhibited different transcriptional responses in these pathways, indicating flexibility and complexity of interactions in the evolution of the mechanisms underlying the hypoxia tolerance phenotype. The variation in the hypoxia-induced transcription of genes across species with similar hypoxia tolerance suggests that similar whole-animal phenotypes can emerge from divergent evolutionary paths that may affect metabolically important functions.
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http://dx.doi.org/10.1186/s12862-018-1275-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215679PMC
November 2018

Mitochondrial responses to anoxia exposure in red eared sliders (Trachemys scripta).

Comp Biochem Physiol B Biochem Mol Biol 2018 Oct 3;224:71-78. Epub 2018 Feb 3.

Department of Zoology, The University of British Columbia, 6270 University Blvd, Vancouver V6T 1Z4, British Columbia, Canada. Electronic address:

When deprived oxygen, mitochondria from most vertebrates transform from the main site of ATP production to the dominant site of cellular ATP use due to the reverse functioning of the F1FO-ATPase (complex V). The anoxia-tolerant freshwater turtle Trachemys scripta however, has previously been shown to inhibit complex V activity in heart and brain in response to anoxia exposure, but the regulatory mechanism is unknown. To gain insight into the putative regulatory mechanisms underlying the anoxia-induced inhibition of complex V in T. scripta, we examined the effects of two weeks anoxia exposure at 4 °C on the mitochondrial proteome and candidate mechanisms that have been shown to regulate complex V in other organisms. In T. scripta, we confirmed that anoxia exposure resulted in a >80% inhibition of complex V in heart, brain and liver. Incubation of mitochondria with the nitric oxide donor, s-nitrosoglutathione, did not affect complex V activity despite showing the expected inhibition in mice. Proteomics analysis showed anoxia-induced decreases in three peripheral stalk subunits of complex V, possibly pointing to a unique site of regulation. Proteomics analysis also revealed differential expression of numerous enzymes involved with the electron transport system, the tricarboxylic acid cycle, as well as lipid and amino acid metabolism in response to anoxia exposure.
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http://dx.doi.org/10.1016/j.cbpb.2018.01.005DOI Listing
October 2018

Naked mole rat brain mitochondria electron transport system flux and H leak are reduced during acute hypoxia.

J Exp Biol 2018 02 20;221(Pt 4). Epub 2018 Feb 20.

Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4.

Mitochondrial respiration and ATP production are compromised by hypoxia. Naked mole rats (NMRs) are among the most hypoxia-tolerant mammals and reduce metabolic rate in hypoxic environments; however, little is known regarding mitochondrial function during hypoxia exposure in this species. To address this knowledge gap, we asked whether the function of NMR brain mitochondria exhibits metabolic plasticity during acute hypoxia. Respirometry was utilized to assess whole-animal oxygen consumption rates and high-resolution respirometry was utilized to assess electron transport system (ETS) function in saponin-permeabilized NMR brain. We found that NMR whole-animal oxygen consumption rate reversibly decreased by ∼85% in acute hypoxia (4 h at 3% O). Similarly, relative to untreated controls, permeabilized brain respiratory flux through the ETS was decreased by ∼90% in acutely hypoxic animals. Relative to carbonyl cyanide -trifluoro-methoxyphenylhydrazone-uncoupled total ETS flux, this functional decrease was observed equally across all components of the ETS except for complex IV (cytochrome oxidase), at which flux was further reduced, supporting a regulatory role for this enzyme during acute hypoxia. The maximum enzymatic capacities of ETS complexes I-V were not altered by acute hypoxia; however, the mitochondrial H gradient decreased in step with the decrease in ETS respiration. Taken together, our results indicate that NMR brain ETS flux and H leak are reduced in a balanced and regulated fashion during acute hypoxia. Changes in NMR mitochondrial metabolic plasticity mirror whole-animal metabolic responses to hypoxia.
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http://dx.doi.org/10.1242/jeb.171397DOI Listing
February 2018

Hypoxia induces selective modifications to the acetylome in the brain of zebrafish (Danio rerio).

Comp Biochem Physiol B Biochem Mol Biol 2018 Oct 5;224:79-87. Epub 2018 Jan 5.

Department of Zoology, The University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada.

Reversible protein acetylation is an important regulatory mechanism for modulating protein function. The cellular protein acetylome is in large part dictated by the cellular redox balance, and in particular [NAD]. While the relationship between hypoxia, redox balance, energy charge and resulting mitochondrial dysfunction has been examined in the context of hypoxia-linked pathologies, little is known about the direct effects of decreases in environmental oxygen on reversible lysine acetylation, and the resulting modifications to mitochondrial metabolism. To address this knowledge gap, we exposed zebrafish (Danio rerio) to 16 h of hypoxia (2.21 kPa) and quantified acetylation levels of 1220 proteins using whole-cell proteomics in samples of brain taken from normoxic and hypoxic zebrafish. In addition, we examined the effects of hypoxia on cytoplasmic and mitochondrial redox status, whole-cell energetics, the activity of the mitochondrial NAD-dependent deacetylase SIRT3, and electron transport chain complex activities to determine if there is an association between hypoxia-induced metabolic disturbances, protein acetylation, and mitochondrial function. Our results (1) reveal several key changes in the acetylation status of proteins in the brain, primarily within the mitochondria; (2) show significant fluctuations in cytoplasmic and mitochondrial redox status within the brain during hypoxia exposure; and (3) provide evidence that lysine acetylation may be related to large changes in electron transport and ATP-synthase complex activities and adenylate status in zebrafish exposed to hypoxic stress. Together, these data provide new insights into the role of protein modifications in mitochondrial metabolism during hypoxia.
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http://dx.doi.org/10.1016/j.cbpb.2017.12.018DOI Listing
October 2018

Metabolic depression and the evolution of hypoxia tolerance in threespine stickleback, .

Biol Lett 2017 Nov;13(11)

Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4.

Anthropogenic increases in global temperature and agricultural runoff are increasing the prevalence of aquatic hypoxia throughout the world. We investigated the potential for a relatively rapid evolution of hypoxia tolerance using two isolated (for less than 11 000 years) populations of threespine stickleback: one from a lake that experiences long-term hypoxia (Alta Lake, British Columbia) and one from a lake that does not (Trout Lake, British Columbia). Loss-of-equilibrium (LOE) experiments revealed that the Alta Lake stickleback were significantly more tolerant of hypoxia than the Trout Lake stickleback, and calorimetry experiments revealed that the enhanced tolerance of Alta Lake stickleback may be associated with their ability to depress metabolic rate (as indicated by metabolic heat production) by 33% in hypoxia. The two populations showed little variation in their capacities for O extraction and anaerobic metabolism. These results reveal that intraspecific variation in hypoxia tolerance can develop over relatively short geological timescales, as can metabolic rate depression, a complex biochemical response that may be favoured in long-term hypoxic environments.
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http://dx.doi.org/10.1098/rsbl.2017.0392DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5719371PMC
November 2017

Ethanol metabolism varies with hypoxia tolerance in ten cyprinid species.

J Comp Physiol B 2018 03 14;188(2):283-293. Epub 2017 Oct 14.

Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada.

During periods of severe hypoxia or anoxia, Carassius spp. are known for their ability to produce ethanol as their anaerobic end product, which diffuses into the environment thereby reducing the osmotic and acidotic load associated with "anaerobic" glycolysis. However, the relationship between alcohol dehydrogenase (ADH) and acetaldehyde dehydrogenase (ALDH) activities, key ethanol metabolizing enzymes, and hypoxia tolerance among Carassius spp. and their closely related non-ethanol-producing cyprinids remains unclear. To address this, we quantified the activity levels of key anaerobic enzymes in liver and muscle in species of cyprinids over 48 h of severe hypoxia exposure (0.7 kPa). As predicted, muscle ADH activity was highest in the two most hypoxia-tolerant species (Carassius spp.), with very low levels present in the other species examined. However, liver ADH activities showed an inverse relationship with hypoxia tolerance, with the most hypoxia-tolerant fish having the lowest ADH activity. There was no correlation between hypoxia tolerance and ALDH and LDH activities in muscle or liver. All species produced lactate, reaching their highest levels after 8 h, but returning to near-baseline levels by 48 h of sustained exposure to hypoxia, suggesting lactate oxidation or depressed ATP demand. Liver glycogen content was not affected by 48 h hypoxia exposure in the most hypoxia-tolerant species, whereas the least tolerant species consumed the majority of the liver glycogen stores, which is probably due to the greater relative hypoxia exposure experienced by these species. Our findings that liver ADH activities were inversely related to hypoxia tolerance suggests that in all but Carassius spp., the ethanol metabolizing pathways in cyprinids is largely similar to that observed in other vertebrates and plays a role in the detoxification of ethanol. Furthermore, conservation of glycogen stores may be the result of metabolic-depressing pathways in the more tolerant species, regardless of the ability to produce ethanol, or adaptations that improve oxygen uptake to reduce metabolic demands due to hypoxia.
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http://dx.doi.org/10.1007/s00360-017-1131-4DOI Listing
March 2018

Evolution of Cytochrome c Oxidase in Hypoxia Tolerant Sculpins (Cottidae, Actinopterygii).

Mol Biol Evol 2017 09;34(9):2153-2162

Department of Zoology, The University of British Columbia, Vancouver, BC, Canada.

Vertebrate hypoxia tolerance can emerge from modifications to the oxygen (O2) transport cascade, but whether there is adaptive variation to O2 binding at the terminus of this cascade, mitochondrial cytochrome c oxidase (COX), is not known. In order to address the hypothesis that hypoxia tolerance is associated with enhanced O2 binding by mitochondria we undertook a comparative analysis of COX O2 kinetics across species of intertidal sculpins (Cottidae, Actinopterygii) that vary in hypoxia tolerance. Our analysis revealed a significant relationship between hypoxia tolerance (critical O2 tension of O2 consumption rate; Pcrit), mitochondrial O2 binding affinity (O2 tension at which mitochondrial respiration was half maximal; P50), and COX O2-binding affinity (apparent Michaelis-Menten constant for O2 binding to COX; Km,app O2). The more hypoxia tolerant species had both a lower mitochondrial P50 and lower COX Km,app O2, facilitating the maintenance of mitochondrial function to a lower O2 tension than in hypoxia intolerant species. Additionally, hypoxia tolerant species had a lower overall COX Vmax but higher mitochondrial COX respiration rate when expressed relative to maximal electron transport system respiration rate. In silico analyses of the COX3 subunit postulated as the entry point for O2 into the COX protein catalytic core, points to variation in COX3 protein stability (estimated as free energy of unfolding) contributing to the variation in COX Km,app O2. We propose that interactions between COX3 and cardiolipin at four amino acid positions along the same alpha-helix forming the COX3 v-cleft represent likely determinants of interspecific differences in COX Km,app O2.
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http://dx.doi.org/10.1093/molbev/msx179DOI Listing
September 2017

Rates of hypoxia induction alter mechanisms of O uptake and the critical O tension of goldfish.

J Exp Biol 2017 07 5;220(Pt 14):2536-2544. Epub 2017 May 5.

Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, British Columbia, Canada V6T 1Z4.

The rate of hypoxia induction (RHI) is an important but overlooked dimension of environmental hypoxia that may affect an organism's survival. We hypothesized that, compared with rapid RHI, gradual RHI will afford an organism more time to alter plastic phenotypes associated with O uptake and subsequently reduce the critical O tension () of the rate of O uptake ( ). We investigated this by determining values for goldfish exposed to short (∼24 min), typical (∼84 min) and long (∼480 min) duration trials to represent different RHIs. Consistent with our predictions, long duration trials yielded significantly lower values (1.0-1.4 kPa) than short and typical duration trials, which did not differ (2.6±0.3 and 2.5±0.2 kPa, respectively). Parallel experiments revealed these time-related shifts in were associated with changes to aspects of the O transport cascade that took place over the hypoxia exposures: gill surface areas and haemoglobin-O binding affinities were significantly higher in fish exposed to gradual RHIs over 480 min than fish exposed to rapid RHIs over 60 min. Our results also revealed that the choice of respirometric technique (i.e. closed versus intermittent) does not affect or routine , despite the significantly reduced water pH and elevated CO and ammonia levels measured following closed-circuit trials of ∼90 min. Together, our results demonstrate that gradual RHIs result in alterations to physiological parameters that enhance O uptake in hypoxic environments. An organism's innate is therefore most accurately determined using rapid RHIs (<90 min) so as to avoid the confounding effects of hypoxic acclimation.
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http://dx.doi.org/10.1242/jeb.154948DOI Listing
July 2017

Subfunctionalization of COX4 paralogs in fish.

Am J Physiol Regul Integr Comp Physiol 2017 05 1;312(5):R671-R680. Epub 2017 Feb 1.

Department of Biology, Queen's University, Kingston, Ontario, Canada; and

Cytochrome oxidase (COX) subunit 4 has two paralogs in most vertebrates. The mammalian COX4-2 gene is hypoxia responsive, and the protein has a disrupted ATP-binding site that confers kinetic properties on COX that distinguish it from COX4-1. The structure-function of COX4-2 orthologs in other vertebrates remains uncertain. Phylogenetic analyses suggest the two paralogs arose in basal vertebrates, but COX4-2 orthologs diverged faster than COX4-1 orthologs. COX4-1/4-2 protein levels in tilapia tracked mRNA levels across tissues, and did not change in hypoxia, arguing against a role for differential post-translational regulation of paralogs. The heart, and to a lesser extent the brain, showed a size-dependent shift from COX4-1 to COX4-2 (transcript and protein). ATP allosterically inhibited both velocity and affinity for oxygen in COX assayed from both muscle (predominantly COX4-2) and gill (predominantly COX4-1). We saw some evidence of cellular and subcellular discrimination of COX4 paralogs in heart. In cardiac ventricle, some non-cardiomyocyte cells were COX positive but lacked detectible COX4-2. Within heart, the two proteins partitioned to different mitochondrial subpopulations. Cardiac subsarcolemmal mitochondria had mostly COX4-1 and intermyofibrillar mitochondria had mostly COX4-2. Collectively, these data argue that, despite common evolutionary origins, COX4-2 orthologs of fish show unique patterns of subfunctionalization with respect to transcriptional and posttranslation regulation relative to the rodents and primates that have been studied to date.
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http://dx.doi.org/10.1152/ajpregu.00479.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451570PMC
May 2017

Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments.

J Exp Biol 2017 Feb 2;220(Pt 4):564-572. Epub 2016 Dec 2.

Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC, Canada V6T 1Z4.

Metabolic rate depression (MRD) has long been proposed as the key metabolic strategy of hypoxic survival, but surprisingly, the effects of changes in hypoxic O tensions (w ) on MRD are largely unexplored. We simultaneously measured the O consumption rate ( ) and metabolic heat of goldfish using calorespirometry to test the hypothesis that MRD is employed at hypoxic w  values and initiated just below , the wbelow which  is forced to progressively decline as the fish oxyconforms to decreasing w Specifically, we used closed-chamber and flow-through calorespirometry together with terminal sampling experiments to examine the effects of w  and time on , metabolic heat and anaerobic metabolism (lactate and ethanol production). The closed-chamber and flow-through experiments yielded slightly different results. Under closed-chamber conditions with a continually decreasing w , goldfish showed a of 3.0±0.3 kPa and metabolic heat production was only depressed at w  between 0 and 0.67 kPa. Under flow-through conditions with w  held at a variety of oxygen tensions for 1 and 4 h, goldfish also initiated MRD between 0 and 0.67 kPa but maintained  to 0.67 kPa, indicating that is at or below this w Anaerobic metabolism was strongly activated at w≤1.3 kPa, but only used within the first hour at 1.3 and 0.67 kPa, as anaerobic end-products did not accumulate between 1 and 4 h exposure. Taken together, it appears that goldfish reserve MRD for near-anoxia, supporting routine metabolic rate at sub-w  values with the help of anaerobic glycolysis in the closed-chamber experiments, and aerobically after an initial (<1 h) activation of anaerobic metabolism in the flow-through experiments, even at 0.67 kPa w.
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http://dx.doi.org/10.1242/jeb.145169DOI Listing
February 2017

Mitochondrial responses to prolonged anoxia in brain of red-eared slider turtles.

Biol Lett 2016 Jan;12(1):20150797

Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4.

Mitochondria are central to aerobic energy production and play a key role in neuronal signalling. During anoxia, however, the mitochondria of most vertebrates initiate deleterious cell death cascades. Nonetheless, a handful of vertebrate species, including some freshwater turtles, are remarkably tolerant of low oxygen environments and survive months of anoxia without apparent damage to brain tissue. This tolerance suggests that mitochondria in the brains of such species are adapted to withstand prolonged anoxia, but little is known about potential neuroprotective responses. In this study, we address such mechanisms by comparing mitochondrial function between brain tissues isolated from cold-acclimated red-eared slider turtles (Trachemys scripta elegans) exposed to two weeks of either normoxia or anoxia. We found that brain mitochondria from anoxia-acclimated turtles exhibited a unique phenotype of remodelling relative to normoxic controls, including: (i) decreased citrate synthase and F1FO-ATPase activity but maintained protein content, (ii) markedly reduced aerobic capacity, and (iii) mild uncoupling of the mitochondrial proton gradient. These data suggest that turtle brain mitochondria respond to low oxygen stress with a unique suite of changes tailored towards neuroprotection.
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http://dx.doi.org/10.1098/rsbl.2015.0797DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4785919PMC
January 2016

The effects of strain and ploidy on the physiological responses of rainbow trout (Oncorhynchus mykiss) to pH 9.5 exposure.

Comp Biochem Physiol B Biochem Mol Biol 2015 May 23;183:22-9. Epub 2014 Dec 23.

Department of Zoology, The University of British Columbia, 6270 University Blvd., Vancouver, BC V6T 1Z4, Canada.

We characterized the physiological effects of exposure to pH9.5 on one domesticated and four wild strains of diploid and triploid juvenile rainbow trout (Oncorhynchus mykiss) over two consecutive years. In the first year, 35-70% of the individuals from the wild strains showed a loss of equilibrium (LOE) at 12 h exposure to pH9.5, with all fish from wild strains experiencing a LOE by 48 h. In contrast, <20% of the domesticated strain showed LOE over the 48 h exposure to pH9.5. In our second experiment, similar strain effects were observed, but far fewer fish showed LOE (≤50% in all strains) over 72 h at pH9.5. In both experiments, there was no effect of ploidy on time to LOE. In the fish that did not show LOE, high pH exposure resulted in significant increases in plasma, brain and muscle ammonia, with no effect of strain or ploidy on the extent of ammonia accumulation. Glutamine accumulated in the brain during high pH exposure, with a stoichiometric decrease in glutamate, but no differences were noted among strains or ploidies. Lactate also accumulated in the plasma to a similar extent in all trout strains and ploidies. Plasma chloride decreased at 24h exposure in all trout strains and ploidies, but recovered by 72 h. No change was observed in plasma sodium. Overall, our data suggest that the domesticated strain of trout is more tolerant of pH9.5 than the wild strains, but these differences in tolerance cannot be explained by our sub-lethal assessment of ammonia balance or ion regulation.
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http://dx.doi.org/10.1016/j.cbpb.2014.12.005DOI Listing
May 2015

Divergent transcriptional patterns are related to differences in hypoxia tolerance between the intertidal and the subtidal sculpins.

Mol Ecol 2014 Dec 27;23(24):6091-103. Epub 2014 Nov 27.

Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, BC, V6T 1Z4, Canada; Bamfield Marine Sciences Centre, 100 Pachena Rd., Bamfield, BC, V0R 1B0, Canada.

Transcriptionally mediated phenotypic plasticity as a mechanism of modifying traits in response to an environmental challenge remains an important area of study. We compared the transcriptional responses to low oxygen (hypoxia) of the hypoxia-tolerant intertidal fish, the tidepool sculpin (Oligocottus maculosus) with the closely related hypoxia-intolerant subtidal fish, the silverspotted sculpin (Blepsias cirrhosus) to determine whether these species use different mechanisms to cope with hypoxia. Individuals from each species were exposed to environmental O(2) tensions chosen to yield a similar level of tissue hypoxia, and gene transcription was assessed in the liver over time. There was an effect of time in hypoxia, where the greatest transcriptional change in the silverspotted sculpin occurred between 3 and 24 h in contrast to the tidepool sculpin where the largest transcriptional change occurred between 24 and 72 h of hypoxia. A number of genes showed similar hypoxia-induced transcription patterns in both species (e.g. genes associated with glycolysis and apoptosis) suggesting they are involved in a conserved hypoxia response. A large set of genes showed divergent transcriptional patterns in the two species, including fatty acid oxidation and oxidative phosphorylation, suggesting that these biological processes may contribute to explaining variation in hypoxia tolerance in these species. When both species were exposed to a single environmental O(2) tension, large transcriptional responses were seen in the hypoxia-intolerant silverspotted sculpin while almost no response was observed in the hypoxia-tolerant tidepool sculpin. Overall, divergent transcription patterns in response to both magnitude and duration of hypoxia provide insights into the processes that may determine an animal's capacity to tolerate frequent bouts of hypoxia in the wild.
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http://dx.doi.org/10.1111/mec.12991DOI Listing
December 2014

Conditioned place avoidance of zebrafish (Danio rerio) to three chemicals used for euthanasia and anaesthesia.

PLoS One 2014 4;9(2):e88030. Epub 2014 Feb 4.

Animal Welfare Program, University of British Columbia, Vancouver, British Columbia, Canada.

Zebrafish are becoming one of the most used vertebrates in developmental and biomedical research. Fish are commonly killed at the end of an experiment with an overdose of tricaine methanesulfonate (TMS, also known as MS-222), but to date little research has assessed if exposure to this or other agents qualifies as euthanasia (i.e. a "good death"). Alternative agents include metomidate hydrochloride and clove oil. We use a conditioned place avoidance paradigm to compare aversion to TMS, clove oil, and metomidate hydrochloride. Zebrafish (n = 51) were exposed to the different anaesthetics in the initially preferred side of a light/dark box. After exposure to TMS zebrafish spent less time in their previously preferred side; aversion was less pronounced following exposure to metomidate hydrochloride and clove oil. Nine of 17 fish exposed to TMS chose not to re-enter the previously preferred side, versus 2 of 18 and 3 of 16 refusals for metomidate hydrochloride and clove oil, respectively. We conclude that metomidate hydrochloride and clove oil are less aversive than TMS and that these agents be used as humane alternatives to TMS for killing zebrafish.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0088030PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3913715PMC
September 2014

Mitochondria from anoxia-tolerant animals reveal common strategies to survive without oxygen.

J Comp Physiol B 2014 Apr 7;184(3):285-302. Epub 2014 Feb 7.

Faculty of Medicine and Human Sciences, University of Manchester, 2.4 Core Technology Facility, 46 Grafton St, Manchester, M139NT, UK,

The mitochondrion plays a critical role in the development of Oxygen (O2)-related diseases. While research has predominantly focused on hypoxia-sensitive mammals as surrogates for humans, the use of animals which have naturally evolved anoxia tolerance has been largely ignored. Remarkably, some animals can live in the complete absence of O2 for days, months and even years, but surprisingly little is currently known about mitochondrial function in these species. In contrast to mammals, mitochondrial function in anoxia-tolerant animals is relatively insensitive to in vitro anoxia and reoxygenation, suggesting that anoxia tolerance transcends to the level of the mitochondria. Furthermore, long-term anoxia is associated with marked changes in the intrinsic properties of the mitochondria from these species, which may afford protection against anoxia-related damage. In the present review, we highlight some of the strategies anoxia-tolerant animals possess to preserve mitochondrial function in the absence of O2. Specifically, we review mitochondrial Ca(2+) regulation, proton leak, redox signaling and mitochondrial permeability transition, in phylogenetically diverse groups of anoxia-tolerant animals. From the strategies they employ, these species emerge as model organisms to illuminate novel interventions to mitigate O2-related mitochondrial dysfunction in humans.
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http://dx.doi.org/10.1007/s00360-014-0806-3DOI Listing
April 2014

Interspecific differences in hypoxia-induced gill remodeling in carp.

Physiol Biochem Zool 2013 Nov-Dec;86(6):727-39. Epub 2013 Sep 23.

Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada; 2Department of Biology, San Diego State University, San Diego, California; 3Laboratory of Evolutionary Physiology and Behavior, Chongqing Key Laboratory of Animal Biology, Chongqing Normal University, Chongqing, China; 4Department of Biology, Queen's University, 116 Barrie Street, Kingston, Ontario K7L 3N6, Canada.

The gills of many fish, but in particular those of crucian carp (Carassius carassius) and goldfish (Carassius auratus), are capable of extensive remodeling in response to changes in oxygen (O2), temperature, and exercise. In this study, we investigated the interspecific variation in hypoxia-induced gill modeling and hypoxia tolerance in 10 closely related groups of cyprinids (nine species, with two strains of Cyprinus carpio). There was significant variation in hypoxia tolerance, measured as the O2 tension (P(O2)) at which fish lost equilibrium (LOEcrit), among the 10 groups of carp. In normoxia, there was a significant, phylogenetically independent relationship between mass-specific gill surface area and LOEcrit, with the more hypoxia-tolerant carp having smaller gills than their less hypoxia-tolerant relatives. All groups of carp, except the Chinese bream (Megalobrama pellegrini), increased mass-specific gill surface area in response to 48 h of exposure to hypoxia (0.7 kPa) through reductions in the interlamellar cell mass (ILCM) volume. The magnitude of the hypoxia-induced reduction in the ILCM was negatively correlated with LOEcrit (and thus positively correlated with hypoxia tolerance), independent of phylogeny. The hypoxia-induced changes in gill morphology resulted in reduced variation in mass-specific gill surface area among species and eliminated the relationship between LOEcrit and mass-specific gill surface area. While behavioral responses to hypoxia differed among the carp groups, there were no significant relationships between hypoxia tolerance and the Po2 at which aquatic surface respiration (ASR) was initiated or the total number of ASR events observed during progressive hypoxia. Our results are the first to show that the extent of gill remodeling in cyprinids is associated with hypoxia tolerance in a phylogenetically independent fashion.
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http://dx.doi.org/10.1086/673180DOI Listing
June 2014

Migration, mitochondria, and the yellow-rumped warbler.

Evolution 2014 Jan 16;68(1):241-55. Epub 2013 Sep 16.

Department of Zoology and Biodiversity Research Centre, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada.

Discordance between mitochondrial and nuclear DNA has been noted in many systems. Asymmetric introgression of mitochondria is a common cause of such discordances, although in most cases the drivers of introgression are unknown. In the yellow-rumped warbler, evidence suggests that mtDNA from the eastern, myrtle warbler, has introgressed across much of the range of the western form, the Audubon's warbler. Within the southwestern United States myrtle mtDNA comes into contact with another clade that occurs in the Mexican black-fronted warbler. Both northern forms exhibit seasonal migration, whereas black-fronted warblers are nonmigratory. We investigated the link between mitochondrial introgression, mitochondrial function, and migration using novel genetic, isotopic, biochemical, and phenotypic data obtained from populations in the transition zone. Isotopes suggest the zone is coincident with a shift in migration, with individuals in the south being resident and populations further north becoming increasingly more migratory. Mitochondrial respiration in flight muscles demonstrates that myrtle-type individuals have a significantly greater acceptor control ratio of mitochondria, suggesting it may be more metabolically efficient. To our knowledge this is the first time this type of intraspecific variation in mitochondrial respiration has been measured in wild birds and we discuss how such mitochondrial adaptations may have facilitated introgression.
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http://dx.doi.org/10.1111/evo.12260DOI Listing
January 2014

Beating oxygen: chronic anoxia exposure reduces mitochondrial F1FO-ATPase activity in turtle (Trachemys scripta) heart.

J Exp Biol 2013 Sep;216(Pt 17):3283-93

Department of Zoology, The University of British Columbia, Vancouver, BC, Canada.

The freshwater turtle Trachemys scripta can survive in the complete absence of O2 (anoxia) for periods lasting several months. In mammals, anoxia leads to mitochondrial dysfunction, which culminates in cellular necrosis and apoptosis. Despite the obvious clinical benefits of understanding anoxia tolerance, little is known about the effects of chronic oxygen deprivation on the function of turtle mitochondria. In this study, we compared mitochondrial function in hearts of T. scripta exposed to either normoxia or 2 weeks of complete anoxia at 5°C and during simulated acute anoxia/reoxygenation. Mitochondrial respiration, electron transport chain activities, enzyme activities, proton conductance and membrane potential were measured in permeabilised cardiac fibres and isolated mitochondria. Two weeks of anoxia exposure at 5°C resulted in an increase in lactate, and decreases in ATP, glycogen, pH and phosphocreatine in the heart. Mitochondrial proton conductance and membrane potential were similar between experimental groups, while aerobic capacity was dramatically reduced. The reduced aerobic capacity was the result of a severe downregulation of the F1FO-ATPase (Complex V), which we assessed as a decrease in enzyme activity. Furthermore, in stark contrast to mammalian paradigms, isolated turtle heart mitochondria endured 20 min of anoxia followed by reoxygenation without any impact on subsequent ADP-stimulated O2 consumption (State III respiration) or State IV respiration. Results from this study demonstrate that turtle mitochondria remodel in response to chronic anoxia exposure and a reduction in Complex V activity is a fundamental component of mitochondrial and cellular anoxia survival.
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http://dx.doi.org/10.1242/jeb.087155DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4074260PMC
September 2013

Effects of fatty acid provision during severe hypoxia on routine and maximal performance of the in situ tilapia heart.

J Comp Physiol B 2013 Aug 29;183(6):773-85. Epub 2013 Mar 29.

Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC V6T 1Z4, Canada.

The ability to maintain stable cardiac function during environmental hypoxia exposure is crucial for hypoxia tolerance in animals and depends upon the maintenance of cardiac energy balance as well as the state of the heart's extracellular environment (e.g., availability of metabolic fuels). Hypoxic depression of plasma [non-esterified fatty acids] (NEFA), an important cardiac aerobic fuel, is a common response in many species of hypoxia-tolerant fishes, including tilapia. We tested the hypothesis that decreased plasma [NEFA] is important for maintaining stable cardiac function during and following hypoxia exposure, based on the premise that continued reliance upon cardiac fatty acid metabolism under such conditions could impair cardiac function. We examined the effect of severe hypoxia exposure (PO2 < 0.2 kPa) on routine and maximum performance of the in situ perfused tilapia heart under conditions of routine (400 μmol L(-1)) and low (75 μmol L(-1)) [palmitate], which mimicked the in vivo levels of plasma [NEFA] found in normoxic and hypoxic tilapia, respectively. Under both concentrations of palmitate, the in situ tilapia heart showed exceptional hypoxic performance as a result of a high maximum glycolytic potential, confirming our previous results using a perfusate without fatty acids. We additionally provide evidence suggesting that non-contractile ATP demand is depressed in tilapia heart during hypoxia exposure. Cardiac performance during and following severe hypoxia exposure was unaffected by the level of palmitate. Thus, we conclude that hypoxic depression of plasma [NEFA] in fishes does not play a role in cardiac hypoxia tolerance.
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http://dx.doi.org/10.1007/s00360-013-0750-7DOI Listing
August 2013