Oxidative stress and condition-dependent sexual signals: more than just seeing red

Garratt, Michael; Brooks, Robert

doi:10.1098/rspb.2012.0568

Cited by 86 publications

(86 citation statements)

References 97 publications

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“…Protein thiols were measured as described by Di Monte et al (1984; see protein sulfhydryl groups measure description under Methods section 'Measurement of protein mixed disulfides, protein sulfhydryl groups and protein binding' in their study), altered for use on a plate reader by transferring sample and glutathione standards (for calibration curve) to a 96-well microplate and measuring the absorbance at 405 nm in an automatic microplate reader (Biotek Instruments, Winooski, VT, USA). This adaptation has been used previously (Garratt and Brooks, 2012;Garratt et al, 2013Garratt et al, , 2014.…”

Section: Oxidative Stress Analysismentioning

confidence: 99%

Experimental evidence that litter size imposes an oxidative challenge to offspring

Gibson

Garratt

Brooks

2015

Journal of Experimental Biology

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The post-natal environment in which young develop can substantially impact development, adult phenotype and fitness. In wild mice, competition among litter-mates affects development rate and adult behaviour. We manipulated post-natal litter size in a cross-fostering design to investigate the effects of enlarged and reduced litter sizes on sexual signalling, oxidative stress and the links between them. Oxidative stress causes somatic damage that can limit reproductive success and lifespan, and is predicted to mediate investment in life-history traits, including sexual signals. We predicted that litter enlargement would cause an increase in potential oxidative stress, inhibit growth and reduce sexual signalling in male mice. Males reared in enlarged litters were smaller at weaning and, despite rapid growth immediately after weaning, remained smaller at 10 weeks of age than those reared in smaller litters. Females from enlarged litters were consistently smaller throughout post-weaning development and showed no increase in growth rate compared with females from reduced litters. In enlarged litters, protein thiol concentration was lower at weaning in the liver and kidneys, with this trend continuing at 10 weeks of age in the kidneys only. Aconitase enzyme activity was also lower in mice from enlarged litters at weaning and 10 weeks of age in the kidneys. Male mice from enlarged litters scent marked more frequently and had larger preputial glands than those from reduced litters, indicating greater sexual signalling investment irrespective of this increased oxidative challenge. The results of this study are the first to reveal oxidative costs of developmental stress in small mammals.

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Section: Oxidative Stress Analysismentioning

confidence: 99%

Experimental evidence that litter size imposes an oxidative challenge to offspring

Gibson

Garratt

Brooks

2015

Journal of Experimental Biology

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“…The regulation of oxidative damage may act as an underlying driver of aging or longevity (Montgomery et al, 2012;Selman et al, 2012). Other reviews have focused on the regulation of RS production from an evolutionary perspective (Costantini, 2008(Costantini, , 2014Costantini et al, 2010b;Monaghan et al, 2009;Speakman, 2008;Speakman et al, 2015;Williams et al, 2010), or on the role of RS in conservation physiology (Beaulieu and Costantini, 2014;Isaksson, 2010), in signaling (Garratt and Brooks, 2012) and as an important indicator of bird health for field ornithologists (Hutton and McGraw, 2016;, or on the importance of dietary antioxidants for wild animals (e.g. Beaulieu and Schaefer, 2013;Catoni et al, 2008b).…”

Section: Introductionmentioning

confidence: 99%

The role of the antioxidant system during intense endurance exercise: lessons from migrating birds

Cooper-Mullin

McWilliams

2016

Journal of Experimental Biology

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During migration, birds substantially increase their metabolic rate and burn fats as fuel and yet somehow avoid succumbing to overwhelming oxidative damage. The physiological means by which vertebrates such as migrating birds can counteract an increased production of reactive species (RS) are rather limited: they can upregulate their endogenous antioxidant system and/or consume dietary antioxidants ( prophylactically or therapeutically). Thus, birds can alter different components of their antioxidant system to respond to the demands of long-duration flights, but much remains to be discovered about the complexities of RS production and antioxidant protection throughout migration. Here, we use bird migration as an example to discuss how RS are produced during endurance exercise and how the complex antioxidant system can protect against cellular damage caused by RS. Understanding how a bird's antioxidant system responds during migration can lend insights into how antioxidants protect birds during other life-history stages when metabolic rate may be high, and how antioxidants protect other vertebrates from oxidative damage during endurance exercise.

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“…The first hypothesis suggests that metabolically costly sexual signals may reveal oxidative stress because individuals with poor antioxidant defense (associated with oxidative stress) are less able to protect against the additional ROS-induced damage generated by signal expression (5). This increased oxidative damage may produce costs to sexual signaling that outweigh the fitness benefits expected in return, making investment in these traits unprofitable for individuals with high oxidative stress (15). The second hypothesis suggests that oxidative stress may impair bioenergetic function, reducing the ability of animals to produce energy efficiently.…”

Section: Significancementioning

confidence: 99%

“…The second hypothesis suggests that oxidative stress may impair bioenergetic function, reducing the ability of animals to produce energy efficiently. This would be expected to limit the amount of energy available to allocate to metabolically costly sexual signals (15). By examining changes in markers of oxidative stress, whole-body metabolism, and bioenergetic function in both standard and territorial environments, we were able to explore the validity of these hypotheses in relation to mammalian scent communication.…”

Section: Significancementioning

confidence: 99%

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Superoxide dismutase deficiency impairs olfactory sexual signaling and alters bioenergetic function in mice

Garratt¹,

Pichaud²,

Glaros

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Oxidative stress (an overproduction of reactive oxygen species in relation to defense mechanisms) may restrict investment in life history traits, such as growth, reproduction, lifespan, and the production of sexual signals to attract mates. The constraint on sexual signaling by oxidative stress is of particular interest because it has been proposed as a mechanism ensuring that only good-quality males produce the most attractive sexual signals. Despite these predictions, evidence supporting this theory is, at best, equivocal. We used a superoxide dismutase knockout mouse to demonstrate that oxidative stress directly impairs investment in morphological (preputial glands) and molecular (major urinary proteins) components of olfactory signaling essential for mate attraction. By maintaining males in a much more competitive environment than usual for mouse laboratory experiments, we also revealed a range of phenotypes of superoxide dismutase deficiency not observed in previous studies of this mouse model. This range included impaired bioenergetic function, which was undetectable in the control environment of this study. We urge further examination of model organisms in seminatural conditions and more competitive laboratory environments, as important phenotypes can be exposed under these more demanding conditions.L ife history theory is based on the premise that physiological constraints limit investment in life history components. These constraints are expected to generate the negative correlations commonly observed between these traits on an interspecies level (1). Within species, individuals also differ in their capacity to invest in different traits (2), although the physiological causes of this variation remain largely elusive.Oxidative stress occurs as a consequence of an overproduction of reactive oxygen species (ROS) in relation to defense mechanisms (3). Because ROS are produced as a by-product of oxidative phosphorylation, investment in energetically demanding life history traits has been predicted to increase oxidative stress, which may then constrain investment in other areas (4, 5). Ecological research in wild animals has provided correlative evidence for a link between oxidative stress and investment in traits, such as growth (6), reproduction (7,8), and lifespan (7). Early evidence linking oxidative stress to variation in lifespan within (9) and between species (10) led to the development of genetically modified antioxidant enzyme knockout animals, allowing precise tests of the effects of these pathways on lifespan under controlled laboratory conditions (11). These tests concluded that oxidative stress does not play a major role in governing the lifespan of laboratory animals (11).As in the case of lifespan, sexual signals show considerable among-individual variation and can correlate with oxidative stress. Sexual signals are often condition-dependent in expression, such that only good-quality signalers express the largest or most elaborate sexual signals (12). These signaling systems only evolve and rem...

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Oxidative stress and condition-dependent sexual signals: more than just seeing red

Cited by 86 publications

References 97 publications

Experimental evidence that litter size imposes an oxidative challenge to offspring

Experimental evidence that litter size imposes an oxidative challenge to offspring

The role of the antioxidant system during intense endurance exercise: lessons from migrating birds

Superoxide dismutase deficiency impairs olfactory sexual signaling and alters bioenergetic function in mice

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