Effect of growth trajectories on adult performance and lifespan in three-spined sticklebacks

Lee, Who Seung (2010) Effect of growth trajectories on adult performance and lifespan in three-spined sticklebacks. PhD thesis, University of Glasgow.

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Changes in environmental conditions in early life can cause changes in the tempo and pattern of growth and development in animals. Natural selection favours processes that enable animals to make decisions that maximise Darwinian fitness. These decisions are influenced by trade-offs between current and future benefits. An episode of poor conditions (i.e. reduced nutrition, low temperature and changes in photoperiod) is generally linked to a slowing of growth. If adequate conditions are restored after this episode, growth rate is accelerated and normal adult size can be reached; in other words, ‘compensatory’ growth occurs. Compensatory growth has benefits in enabling a return to the typical size-at-age growth trajectory. Although this ability to alter growth rate provides a degree of adaptability, there is now increasing evidence that resource allocation to rapid growth carries various long-term costs. While there is experimental evidence that poor environmental conditions in early life can induce subsequent compensatory growth, little is known about the long-term effects of compensatory growth on locomotor and reproductive performance, and on lifespan.
In this thesis, I investigated how different growth trajectories affected subsequent performance (i.e. locomotory capability, reproduction and lifespan), and how any such effects were influenced by the perceived time until the key life history event of reproduction. Using juvenile three-spined sticklebacks (Gasterosteus aculeatus), I showed that temperature manipulations early in life in three temperature treatments (low, intermediate and high, independent of food supply) or food restriction (with a constant temperature) affected skeletal growth trajectory not only during the manipulation itself, but also during a subsequent compensatory phase. To investigate the effects of time of year, all experimental groups of temperature and food manipulations were replicated at different seasonal periods (= Winter or Spring); to manipulate apparent time of year while holding initial size and maturity constant, a photoperiod manipulation was also undertaken at both seasonal times (ambient or delayed photoperiod).
While there was compensatory growth (i.e. accelerated growth) in the food manipulation, temperature manipulations induced both positive compensatory growth (i.e. growth acceleration following exposure to low temperature) and also ‘negative’ compensatory growth (decelerated growth following exposure to high temperature). The outcome of these changes was that fish in all treatment groups reached the same average size by sexual maturity, despite having different growth patterns. However, early growth trajectories influenced both pre-breeding swimming endurance and its decline over the course of the breeding season, such that swimming ability was negatively correlated with compensatory growth whereas ‘negative’ compensatory growth reduced swimming ability less (Chapter 2). Reproductive investment (males: sexual ornaments and ability to build nests; females: first clutch size and mean egg size) was negatively affected by compensatory growth; positive effects of ‘negative’ compensatory growth on reproduction were found (Chapter 3). Interestingly, the effects of growth rate on subsequent swimming and reproductive performance were greater when the perceived, or actual, time until the breeding season was shorter (Chapter 2 and 3). These results implied that increased metabolic rates and cellular damage (e.g. oxidative stress) induced by compensatory growth negatively affected subsequent performance, while decelerated growth reduced the damage levels and so later performance was less affected.
Under food manipulation, there were similar patterns: compensatory growth (i.e. accelerated growth) negatively affected locomotor and reproductive performance and the time until the breeding season altered the effects on performance (Chapter 4). To further examine trade-offs between growth rate and fitness parameters such as future reproductive investment and rates of senescence, I developed four theoretical models of increasing complexity with different growth-damage scenarios, ranging from assuming that the animal maximises growth regardless of any costs, through assuming a relationship between growth rate and mortality risk, to assuming growth leads to damage accumulation and that the animal is able to apportion resources between somatic growth, gonadal growth and investment in repair of damage. The models predicted that growth trajectories strongly influenced future reproductive investment irrespective of body size at the time of breeding, presumably due to the effects of damage accumulation in the run up to the breeding season; the predictions of the most complex model were closest to the experimental data on egg production (Chapter 5).
Lifespan was different among treatment groups and also influenced by early growth trajectories. Compensatory growth negatively affected lifespan whereas ‘negative’ compensatory growth extended lifespan. Lifespan in female sticklebacks was positively related to egg production. Male sticklebacks lived for a shorter time when they showed less growth between their first and second breeding seasons, and a greater change in the duration of having a red throat between the first and second breeding season (an indicator of reproductive senescence). The costs of compensation were strongest when the perceived time until breeding was shortest (Chapter 6).
Consequently, this thesis shows that environment conditions in early life have substantial effects on subsequent performances and lifespan. Moreover, results in this thesis strongly support the time-stress hypothesis, that is the time available until the onset of a key life history event, in this case reproduction, influences outcomes.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: Activity, Allocation, Compensatory Growth, Dynamic State Dependent Model, Lifespan, Life History Strategy, Reproductive Investment, Photoperiod, Swim, Temperature
Subjects: Q Science > QH Natural history > QH301 Biology
Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences
Supervisor's Name: Monaghan, Professor Pat, Metcalfe, Professor Neil B. and Mangel, Professor Marc
Date of Award: 2010
Depositing User: Dr Who-Seung Lee
Unique ID: glathesis:2010-2294
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 07 Dec 2010
Last Modified: 10 Dec 2012 13:53
URI: https://theses.gla.ac.uk/id/eprint/2294

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