Oxidative stress is a potential cost of breeding in male and female northern elephant seals

Summary The trade‐off between current reproductive effort and survival is a key concept of life‐history theory. A variety of studies support the existence of this trade‐off, but the underlying physiological mechanisms are not well understood. Oxidative stress has been proposed as a potential mechani...

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Veröffentlicht in:Functional ecology 2015-03, Vol.29 (3), p.367-376
Hauptverfasser: Sharick, Jeffrey T., Vazquez-Medina, Jose P., Ortiz, Rudy M., Crocker, Daniel E.
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container_end_page 376
container_issue 3
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container_title Functional ecology
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creator Sharick, Jeffrey T.
Vazquez-Medina, Jose P.
Ortiz, Rudy M.
Crocker, Daniel E.
description Summary The trade‐off between current reproductive effort and survival is a key concept of life‐history theory. A variety of studies support the existence of this trade‐off, but the underlying physiological mechanisms are not well understood. Oxidative stress has been proposed as a potential mechanism underlying the observed inverse relationship between reproductive investment and life span. Prolonged fasting is associated with oxidative stress including increases in the production of reactive oxygen species (ROS), oxidative damage and inflammation. Northern elephant seals (NES) undergo prolonged fasts while maintaining high metabolic rates during breeding. We investigated NES of both sexes to assess oxidative stress associated with extended breeding fasts. We measured changes in the plasma activity or concentrations of markers for oxidative stress in 30 adult male and 33 adult female NES across their 1–3 month breeding fasts. Markers assessed included a pro‐oxidant enzyme, several antioxidant enzymes, markers for oxidative damage to lipids, proteins and DNA and markers for systemic inflammation. Plasma xanthine oxidase (XO), a pro‐oxidant enzyme that increases production of oxidative radicals, and several protective antioxidant enzymes increased over breeding in both sexes. Males showed increased oxidative damage to lipids and DNA and increased systemic inflammation, while oxidative damage to proteins declined across breeding. In contrast, females showed no oxidative damage to lipids or DNA or changes in inflammation but showed increases in oxidative damage to proteins. XO activity, antioxidant enzymes, oxidative damage markers and inflammatory markers were strongly correlated in males but these relationships were weaker or non‐existent in females. Northern elephant seals provide evidence for oxidative stress as a physiological cost of reproduction in a capital breeding mammal. Both sexes strongly up‐regulated antioxidant defences during breeding. Despite this response, and in contrast to similar duration non‐breeding fasts in previous studies on conspecifics, there was evidence of oxidative damage to tissues. These data demonstrate the utility of using plasma markers to examine oxidative stress but also suggest the necessity of measuring a broad suite of plasma markers to assess systemic oxidative stress. Lay Summary
doi_str_mv 10.1111/1365-2435.12330
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A variety of studies support the existence of this trade‐off, but the underlying physiological mechanisms are not well understood. Oxidative stress has been proposed as a potential mechanism underlying the observed inverse relationship between reproductive investment and life span. Prolonged fasting is associated with oxidative stress including increases in the production of reactive oxygen species (ROS), oxidative damage and inflammation. Northern elephant seals (NES) undergo prolonged fasts while maintaining high metabolic rates during breeding. We investigated NES of both sexes to assess oxidative stress associated with extended breeding fasts. We measured changes in the plasma activity or concentrations of markers for oxidative stress in 30 adult male and 33 adult female NES across their 1–3 month breeding fasts. Markers assessed included a pro‐oxidant enzyme, several antioxidant enzymes, markers for oxidative damage to lipids, proteins and DNA and markers for systemic inflammation. Plasma xanthine oxidase (XO), a pro‐oxidant enzyme that increases production of oxidative radicals, and several protective antioxidant enzymes increased over breeding in both sexes. Males showed increased oxidative damage to lipids and DNA and increased systemic inflammation, while oxidative damage to proteins declined across breeding. In contrast, females showed no oxidative damage to lipids or DNA or changes in inflammation but showed increases in oxidative damage to proteins. XO activity, antioxidant enzymes, oxidative damage markers and inflammatory markers were strongly correlated in males but these relationships were weaker or non‐existent in females. Northern elephant seals provide evidence for oxidative stress as a physiological cost of reproduction in a capital breeding mammal. Both sexes strongly up‐regulated antioxidant defences during breeding. Despite this response, and in contrast to similar duration non‐breeding fasts in previous studies on conspecifics, there was evidence of oxidative damage to tissues. These data demonstrate the utility of using plasma markers to examine oxidative stress but also suggest the necessity of measuring a broad suite of plasma markers to assess systemic oxidative stress. 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A variety of studies support the existence of this trade‐off, but the underlying physiological mechanisms are not well understood. Oxidative stress has been proposed as a potential mechanism underlying the observed inverse relationship between reproductive investment and life span. Prolonged fasting is associated with oxidative stress including increases in the production of reactive oxygen species (ROS), oxidative damage and inflammation. Northern elephant seals (NES) undergo prolonged fasts while maintaining high metabolic rates during breeding. We investigated NES of both sexes to assess oxidative stress associated with extended breeding fasts. We measured changes in the plasma activity or concentrations of markers for oxidative stress in 30 adult male and 33 adult female NES across their 1–3 month breeding fasts. Markers assessed included a pro‐oxidant enzyme, several antioxidant enzymes, markers for oxidative damage to lipids, proteins and DNA and markers for systemic inflammation. Plasma xanthine oxidase (XO), a pro‐oxidant enzyme that increases production of oxidative radicals, and several protective antioxidant enzymes increased over breeding in both sexes. Males showed increased oxidative damage to lipids and DNA and increased systemic inflammation, while oxidative damage to proteins declined across breeding. In contrast, females showed no oxidative damage to lipids or DNA or changes in inflammation but showed increases in oxidative damage to proteins. XO activity, antioxidant enzymes, oxidative damage markers and inflammatory markers were strongly correlated in males but these relationships were weaker or non‐existent in females. Northern elephant seals provide evidence for oxidative stress as a physiological cost of reproduction in a capital breeding mammal. Both sexes strongly up‐regulated antioxidant defences during breeding. Despite this response, and in contrast to similar duration non‐breeding fasts in previous studies on conspecifics, there was evidence of oxidative damage to tissues. These data demonstrate the utility of using plasma markers to examine oxidative stress but also suggest the necessity of measuring a broad suite of plasma markers to assess systemic oxidative stress. 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A variety of studies support the existence of this trade‐off, but the underlying physiological mechanisms are not well understood. Oxidative stress has been proposed as a potential mechanism underlying the observed inverse relationship between reproductive investment and life span. Prolonged fasting is associated with oxidative stress including increases in the production of reactive oxygen species (ROS), oxidative damage and inflammation. Northern elephant seals (NES) undergo prolonged fasts while maintaining high metabolic rates during breeding. We investigated NES of both sexes to assess oxidative stress associated with extended breeding fasts. We measured changes in the plasma activity or concentrations of markers for oxidative stress in 30 adult male and 33 adult female NES across their 1–3 month breeding fasts. Markers assessed included a pro‐oxidant enzyme, several antioxidant enzymes, markers for oxidative damage to lipids, proteins and DNA and markers for systemic inflammation. Plasma xanthine oxidase (XO), a pro‐oxidant enzyme that increases production of oxidative radicals, and several protective antioxidant enzymes increased over breeding in both sexes. Males showed increased oxidative damage to lipids and DNA and increased systemic inflammation, while oxidative damage to proteins declined across breeding. In contrast, females showed no oxidative damage to lipids or DNA or changes in inflammation but showed increases in oxidative damage to proteins. XO activity, antioxidant enzymes, oxidative damage markers and inflammatory markers were strongly correlated in males but these relationships were weaker or non‐existent in females. Northern elephant seals provide evidence for oxidative stress as a physiological cost of reproduction in a capital breeding mammal. Both sexes strongly up‐regulated antioxidant defences during breeding. Despite this response, and in contrast to similar duration non‐breeding fasts in previous studies on conspecifics, there was evidence of oxidative damage to tissues. These data demonstrate the utility of using plasma markers to examine oxidative stress but also suggest the necessity of measuring a broad suite of plasma markers to assess systemic oxidative stress. Lay Summary</abstract><cop>England</cop><pub>Wiley</pub><pmid>25983364</pmid><doi>10.1111/1365-2435.12330</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record>
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source Wiley Free Archive; Wiley Online Library Journals; JSTOR; EZB Electronic Journals Library
subjects Animal physiological ecology
Antioxidants
Aquatic mammals
Breeding
Conspecifics
Damage
Deoxyribonucleic acid
DNA
DNA damage
Enzymes
fasting
Females
Inflammation
Life span
life‐history theory
lipid peroxidation
Lipids
Males
Markers
Metabolic rate
Mirounga
Oxidants
Oxidation
Oxidative stress
Oxidizing agents
Physiology
pinnipeds
Plasma
Proteins
Reactive oxygen species
reproduction
Reproduction (biology)
Reproductive effort
Seals
Xanthine oxidase
title Oxidative stress is a potential cost of breeding in male and female northern elephant seals
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