Dietary effects on adult performance and oxidative stress in three-spined sticklebacks

Stewart, Lyndsey A. E. (2014) Dietary effects on adult performance and oxidative stress in three-spined sticklebacks. PhD thesis, University of Glasgow.

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Nutritional conditions during early life can strongly influence the development of an organism in terms of immediate effects on early growth rates but also by shaping key life history traits later. After a period of nutritional deficit in early life, some animals have been found to accelerate their growth to compensate for the bad start once conditions have improved. There is experimental evidence demonstrating that compensatory growth can carry associated long-term costs, such as reduced locomotory capability and reduced investment in reproduction. Further, it has been proposed that oxidative stress may play an integral role in evoking these costs, as a result of a higher metabolic activity during compensatory growth. However, there is currently little literature available to attest this. Dietary-acquired antioxidants are proposed to support the endogenous antioxidant system in preventing oxidative stress and are therefore suggested to mediate life history trade-offs. In this thesis, resveratrol and carotenoids (potential antioxidants) were supplemented in the diets of three-spined sticklebacks Gasterosteus aculeatus in order to assess whether they were able to mitigate the negative effects associated with compensatory growth by reducing oxidative stress. Two important components of oxidative stress, antioxidant enzyme activity levels and oxidative damage were measured.

This thesis showed that food restrictions early in life resulted in a slowing of growth which was subsequently fully compensated for by acceleration in growth once food conditions were restored. Despite adopting different growth patterns, these fish achieved the same average size by sexual maturity as their control growth peers. However, compensatory growth was found to result in significant costs in later life including reduced cognitive and locomotor performance (Chapter 2). Additionally, it was demonstrated that food supplemented with resveratrol had some beneficial effect on cognitive performance in comparison with same-age controls (Chapter 2). However, resveratrol and carotenoid manipulations did not influence locomotor performance (Chapter 2). This result implies that dietary antioxidants were unable to offset the damage to swimming performance caused by compensatory growth, and that their generally beneficial effects in the diet do not affect all aspects of performance similarly, or to the same extent. Both dietary resveratrol and carotenoids influenced oxidative stress status (Chapter 3). Their role in the antioxidant system appears important and complex in that there were several statistical interactions between these dietary antioxidants and endogenous antioxidant enzyme levels. These enzymes play key roles in the defence of reactive oxygen species (Chapter 3). Fish supplemented with a diet higher in carotenoids were found to have reduced levels of oxidative damage to proteins (Chapter 3). This result suggests that although carotenoids appear to be unimportant antioxidants for birds, these findings should not be generalised across all taxa.

Carotenoid and resveratrol availability influenced female reproductive investment (Chapter 3). Females on a diet supplemented with carotenoids had larger clutches suggesting that carotenoids played a positive role in their reproduction (Chapter 3). However, this was only apparent when the fish had not also been supplemented with resveratrol, suggesting that resveratrol may have imposed a detrimental effect on egg production (Chapter 3). Further, male reproductive investment in sexual ornamentation and nest building ability was also influenced by these dietary antioxidants in a similar fashion (Chapter 4: males fed a diet higher in carotenoids had significantly brighter throats at two crucial stages of the breeding season, while resveratrol had no positive effects on the intensity of the males’ red throat signals). This is contrary to the so-called Red Herring hypothesis which suggests that carotenoid-based sexual signals advertise not the carotenoids themselves but other colourless antioxidants. In addition, males fed a diet lower in carotenoids took longer to both begin and complete nest building, whilst resveratrol had no influence on any aspects of nest building (Chapter 4).

The process of mate choice has been suggested to be costly in many species, since the assessment and comparison of potential mates is an energetically demanding process and hence likely to increase oxidative stress. Therefore, it was predicted that resveratrol would facilitate active mate choice in females through beneficial effects associated with its antioxidant properties. Indeed, females supplemented with resveratrol spent significantly more time associating with males than females that had not been fed resveratrol (Chapter 5). These female mate-choice experiments also demonstrated that resveratrol and compensatory growth did not impact male attractiveness (Chapter 5), suggesting that the females did not receive any alternative (and potentially important) mate cues mediated by resveratrol that were independent of the carotenoid-based signal.

There has been growing evidence in the literature demonstrating that resveratrol has neuroprotective properties, therefore reducing age-related reduction in cognitive performance, and this was also supported in the results of this thesis produced in Chapter 2. Chapter 6 investigated whether the supplementation of resveratrol and carotenoids reduced the rate of ageing in three-spined sticklebacks in terms of exploratory and anxiety-related behaviour in an open field test, measured during early life and again in adulthood. However, in contrast to expectations, males that were not fed resveratrol had the greatest increase in exploratory activity across the experimental period (Chapter 6).

Overall, this thesis demonstrates that dietary manipulation with resveratrol (alongside carotenoids) affected numerous life history traits throughout the three-spined stickleback’s lifespan. The evidence produced in this thesis strongly suggests that numerous aspects of an organism’s performance can be affected by key nutrients, over and above calorie intake which is often misconceived as having unprecedented importance. These effects can be subtle in some scenarios and much more complex in others and they do not necessarily generalise terribly well across taxa. Moreover, by measuring oxidative stress status alongside later life performance in these fish, this thesis helps elucidate the precise roles these antioxidants have in influencing oxidative stress and alleviating the negative effects associated with compensatory growth.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: sticklebacks, life histories, resveratrol, carotenoids, oxidative stress
Subjects: Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Supervisor's Name: Lindstorm, Dr. Jan
Date of Award: 3 July 2014
Depositing User: Miss L A E Stewart
Unique ID: glathesis:2014-5160
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 19 Jun 2014 15:27
Last Modified: 19 Jun 2014 15:34

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