Exploring the consequences of mitochondrial differences arising through hybridization of sunfish

Mathers, Katherine E.; Cox, J.A.; Wang, Y.; Moyes, Christopher D.

doi:10.1016/j.cbpa.2014.07.016

Cited by 7 publications

(10 citation statements)

References 26 publications

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“…The ranges of two closely related sunfish, the bluegill (Lepomis macrochirus) and pumpkinseed (Lepomis gibbosus), overlap, but the most northern lakesthe ones that experience the most severe winterfreeze hypoxiacontain only pumpkinseed (Mittelbach, 1984;Farwell et al, 2007). Unsurprisingly, pumpkinseed have repeatedly been shown to be more hypoxia-tolerant than bluegill (Farwell et al, 2007;Mathers et al, 2014;Borowiec et al, 2016). The pumpkinseed's greater tolerance does not appear to result from greater aerobic abilities, as the two species do not differ in P crit (Mathers et al, 2014;Borowiec et al, 2016) or a wide array of underlying mechanisms (Crans et al, 2015;Borowiec et al, 2016).…”

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

“…Unsurprisingly, pumpkinseed have repeatedly been shown to be more hypoxia-tolerant than bluegill (Farwell et al, 2007;Mathers et al, 2014;Borowiec et al, 2016). The pumpkinseed's greater tolerance does not appear to result from greater aerobic abilities, as the two species do not differ in P crit (Mathers et al, 2014;Borowiec et al, 2016) or a wide array of underlying mechanisms (Crans et al, 2015;Borowiec et al, 2016). Where the species do differ is in their capacities for anaerobic metabolism, with the more tolerant pumpkinseed displaying higher lactate dehydrogenase activities in axial muscle (Farwell et al, 2007;Borowiec et al, 2016) and heart (Borowiec et al, 2016) than the less tolerant bluegill.…”

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

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Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies?

Mandic

Regan

2018

Journal of Experimental Biology

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In aquatic environments, hypoxia is a multi-dimensional stressor that can vary in O 2 level (partial pressure of O 2 in water, Pw O2), rate of induction and duration. Natural hypoxic environments can therefore be very different from one another. For the many fish species that have evolved to cope with these different hypoxic environments, survival requires adjusting energy supply and demand pathways to maintain energy balance. The literature describes innumerable ways that fishes combine aerobic metabolism, anaerobic metabolism and metabolic rate depression (MRD) to accomplish this, but it is unknown whether the evolutionary paths leading to these different strategies are determined primarily by species' phylogenetic histories, genetic constraint or their native hypoxic environments. We explored this idea by devising a four-quadrant matrix that bins different aquatic hypoxic environments according to their duration and Pw O2 characteristics. We then systematically mined the literature for well-studied species native to environments within each quadrant, and, for each of 10 case studies, described the species' total hypoxic response (THR), defined as its hypoxia-induced combination of sustained aerobic metabolism, enhanced anaerobic metabolism and MRD, encompassing also the mechanisms underlying these metabolic modes. Our analysis revealed that fishes use a wide range of THRs, but that distantly related species from environments within the same matrix quadrant have converged on similar THRs. For example, environments of moderately hypoxic Pw O2 favoured predominantly aerobic THRs, whereas environments of severely hypoxic Pw O2 favoured MRD. Capacity for aerial emergence as well as predation pressure (aquatic and aerial) also contributed to these responses, in addition to other biotic and abiotic factors. Generally, it appears that the particular type of hypoxia experienced by a fish plays a major role in shaping its particular THR.

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Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies?

Mandic

Regan

2018

Journal of Experimental Biology

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“…Genotyping was conducted to clearly distinguish purebred pumpkinseed from bluegill-pumpkinseed hybrids, which have a very similar outward appearance, using a previously described PCR approach (Near et al, 2004;Mathers et al, 2014). DNA was extracted from small clips of the caudal fin using a REDExtract-N-Amp Tissue PCR Kit (Sigma-Aldrich, Oakville, ON, Canada).…”

Section: Study Animalsmentioning

confidence: 99%

“…that dictate the time to LOE at a constant P O2 . For example, pumpkinseed are able to avoid LOE at ∼2 kPa for a much longer duration than bluegill (Mathers et al, 2014), even though P crit and the P O2 at LOE in our progressive hypoxia protocol were similar between species (∼0.8-1.0 kPa; Fig. 1).…”

Section: Physiological Basis For Hypoxia Tolerancementioning

confidence: 99%

“…For example, the pumpkinseed sunfish [Lepomis gibbosus (Linnaeus 1758)] can tolerate deep hypoxia for longer periods than its congener, the bluegill sunfish [Lepomis macrochirus (Rafinesque 1810)] (Farwell et al, 2007;Mathers et al, 2014). Largemouth bass [Micropterus salmoides (Lacépede 1802)] also appear to be more tolerant of hypoxia than smallmouth bass (Micropterus dolomieu), as largemouth bass maintain higher blood O 2 content in hypoxia and can maintain blood pH at levels of hypoxia that induce a metabolic acidosis in smallmouth bass (Furimsky et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

Crans

Pranckevicius

Scott

2015

Journal of Experimental Biology

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Tradeoffs between hypoxia tolerance and aerobic exercise performance appear to exist in some fish taxa, even though both of these traits are often associated with a high O 2 transport capacity. We examined the physiological basis for this potential tradeoff in four species of sunfish from the family Centrarchidae. Hypoxia tolerance was greatest in rock bass, intermediate in pumpkinseed and bluegill and lowest in largemouth bass, based on measurements of critical O 2 tension (P crit ) and O 2 tension at loss of equilibrium (P O2 at LOE). Consistent with there being a tradeoff between hypoxia tolerance and aerobic exercise capacity, the least hypoxia-tolerant species had the highest critical swimming speed (U crit ) during normoxia and suffered the greatest decrease in U crit in hypoxia. There was also a positive correlation between U crit in normoxia and P O2 at LOE, which remained significant after accounting for phylogeny using phylogenetically independent contrasts. Several sub-organismal traits appeared to contribute to both hypoxia tolerance and aerobic exercise capacity (reflected by traits that were highest in both rock bass and largemouth bass), such as the gas-exchange surface area of the gills, the pH sensitivity of haemoglobin-O 2 affinity, and the activities of lactate dehydrogenase and the gluconeogenic enzyme phosphoenolpyruvate carboxykinase in the liver. Some other suborganismal traits were uniquely associated with either hypoxia tolerance (low sensitivity of haemoglobin-O 2 affinity to organic phosphates, high pyruvate kinase and lactate dehydrogenase activities in the heart) or aerobic exercise capacity (capillarity and fibre size of the axial swimming muscle). Therefore, the cumulative influence of a variety of respiratory and metabolic traits can result in physiological tradeoffs associated with the evolution of hypoxia tolerance and aerobic exercise performance in fish.

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Does chronic exposure to moderate hypoxia affect growth, physiological and oxidative stress biomarkers in adult spotted wolffish (Anarhichas minor) and the hybrid A. minor × A. lupus?

François,

Drouin‐Johnson,

Larouche

et al. 2023

Aquaculture Fish & Fisheries

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Both in their natural habitat (estuaries, marine coastal environment, ocean depths and freshwater lakes) or in captivity conditions (land‐based, open‐sea aquaculture and aquariums), exposure to hypoxia can have direct detrimental effects on fish growth, reproduction, behaviour and health. The objective of this study was to investigate the effects of chronic exposure of spotted wolffish (Anarhichas minor) (∼1.4 kg) and the interspecific hybrid (A. minor × A. lupus) (∼600 g) to moderate hypoxia levels (dissolved oxygen [DO]: 40%, 50% and 60% saturation) in comparison to a normoxia group (control 100%) over a period of 14 weeks at ∼7.5°C. The trials were conducted as a common‐garden experiment (both fish groups reared together) in quadruplicate (4 tanks per DO level = 16 tanks). Fish performance (specific growth rate, feed intake [FI]) and physiological status (condition factor [K] and hepatosomatic index, haematocrit) were monitored at different intervals. The metabolic enzyme activity of citrate synthase (CS), lactate dehydrogenase (LDH) and pyruvate kinase (PK) was measured as well as antioxidant enzymes glutathione reductase and catalase. Oxidative stress indices were assessed by the quantification of thiobarbituric acid reactive substances (TBARS) and the measurement of the enzymatic activity level of aconitase. Significant reduction in growth rate occurred at DO 40%. DO was identified as a major driver of FI. Our results indicate a very strong adaptation to hypoxia as (1) exposures to DO 40% were not severe enough to affect aerobic or anaerobic metabolism capacity or to significantly induce oxidative stress and (2) metabolic organization of the muscle tissue, as expressed by LDH, CS and PK is not affected by DO levels down to 40%. However, at the lowest DO levels (40% and 50%), hybrid fish displayed significantly better growth than the spotted wolffish.

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Exploring the consequences of mitochondrial differences arising through hybridization of sunfish

Cited by 7 publications

References 26 publications

Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies?

Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies?

Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

Does chronic exposure to moderate hypoxia affect growth, physiological and oxidative stress biomarkers in adult spotted wolffish (Anarhichas minor) and the hybrid A. minor × A. lupus?

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