| dc.description.abstract | Multiple traits, including antipredator responses, foraging behaviour, development rate and fecundity, contribute towards an organism’s fitness. These diverse traits interact through shared resources allocated to maximise fitness. Ecological conditions can affect these interactions by driving increased investment in a particular trait at the cost of other traits (inter-trait trade-off). How are these interactions affected when an individual goes through different development stages, which serve different functional roles? What are the consequences for an individual’s fitness in such a complex life cycle?
Complex life cycles have independently evolved multiple times across the tree of life. Yet, we lack a comprehensive evolutionary understanding of these life histories. Each stage within a complex life cycle exhibits unique morphological, physiological, and behavioural traits, serving specific ecological functions and contributing to the organism’s overall fitness. Holometabolous insects are an excellent example of complex life cycles characterised by extreme metamorphosis. Their life cycles involve ontogenetic switches, where extensive tissue remodelling occurs, and some tissues are formed from entirely new sets of cells. These dramatic transitions offer a powerful model system to explore how developmental changes can facilitate or constrain evolutionary adaptations.
My thesis aimed to unravel the ecological and evolutionary dynamics of different stages of a complex life cycle using the holometabolous insect Aedes aegypti. To understand the trade-offs that operate between life stages, I investigated the role of early predation risk conditions across the life cycle of Aedes aegypti. Aedes aegypti has four major stages: egg, larva, pupa and adult. Previous work suggests that ecological conditions experienced by the larval stage affect adult traits. However, we lack knowledge of how early larval conditions affect the pupal stage and the cumulative effects of both stages on adult traits.
I focussed on the motile pupal stage, a transitional stage between larva and adult that is often neglected. By examining its responses to ecological stressors, particularly predation risk, I investigated the adaptive strategies employed during this stage and their broader consequences. Including pupal ecology alongside larval ecology enabled a comprehensive understanding of behavioural and life-history responses and their associated trade-offs across life stages.
Predation is a ubiquitous ecological stressor that has strongly influenced the evolutionary responses of organisms. In this thesis, I used predation risk as an ecological cue to elicit responses in the larval and pupal stages of Aedes aegypti. I then examined the separate and combined non-consumptive effects of predation on key life-history traits. This integrative approach allowed me to address three central questions:
1. How does predation-risk experience during the larval stage influence pupal behaviour?
Rationale: To determine whether the larval experience of risk carries over to the pupal stage, or whether physiological constraints and distinct ecological functions necessitate that pupal response is shaped independently by current conditions rather than by their experience of risk as larvae.
2. Does social context affect the behavioural carryover of predation risk across life stages?
Rationale: Since larvae and pupae often occur in groups, I explored whether group advantages, such as reduced risk per individual, modulate the behavioural carryover of early predation-risk exposure.
3. What are the consequences of predation-risk exposure across immature stages on different life-history traits?
Rationale: Trade-offs, often caused by limited resources, are well-documented between larval and adult stages. I investigated whether these dynamics become more severe when the non-feeding pupal stage is included.
To address these questions, I employed controlled laboratory experiments involving behavioural observations, life history assessments, and biochemical assays, tracking Aedes aegypti across life stages from larva to adult.
In Chapter 2, I investigated whether predation risk experienced during the larval stage influences pupal behaviour, a phenomenon termed behavioural carryover. I predicted that risk-experienced pupae would show distinct behaviours compared with naive pupae, as they would carry information crucial for their survival. Alternatively, I considered the possibility of no behavioural differences between experienced and naive pupae due to evolutionary or physiological constraints on information transfer between life stages.
To test the predictions, I reared larvae under predation-risk (primarily chemical cues) and no-risk conditions and observed pupal behaviour under risk and no-risk environments. I found that pupae with larval predation-risk exposure exhibited significant behavioural changes, such as increased diving frequency and a preference for shallower depths in the no-risk environment. However, when exposed to predation cues, experienced pupae adopted deeper, less frequent dives, whereas naive pupae did not alter their behaviour. Interestingly, these behavioural carryovers were context-dependent, emerging only under resource-limited conditions. Nevertheless, the findings challenge the assumption that metamorphic boundaries prevent the transmission of information across life stages.
Given the context-dependent nature of behavioural carryover observed in Chapter 2, I explored how social context influences this phenomenon in Chapter 3. Being in a group can provide collective risk management benefits, such as the dilution effect, which reduces risk per individual. Therefore, I predicted no behavioural differences between experienced and naive individuals in group settings, as the advantages of group living were expected to render carryover effects from prior risk experience redundant.
To test the prediction, I conducted experiments similar to those in Chapter 2 but recorded individual pupal behaviour in groups of five, i.e., group of experienced vs. group of naive pupae. In group settings, carryover effects disappeared, as both naive and risk-experienced pupae responded similarly to predation cues. This indicates that although pupae are equipped with information on environmental risks through larval learning, being in a group modifies how that information is used. Therefore, it is essential to consider sociality when examining behavioural carryovers across life stages.
In Chapter 4, I investigated the consequences of early predation risk on multiple life-history traits. In complex life cycles, trade-offs between traits (e.g., growth vs. survival) often span different stages, and ecological conditions such as predation risk can influence how resources are allocated across these stages. Using a comparative framework, I examined how predation risk experienced during different stages—larval, pupal, or both—affects life-history traits such as development time, size at metamorphosis, adult longevity and fecundity. I predicted that the costs arising from larval and pupal responses to risk would accumulate, leading to the most adverse trade-off consequences when both stages experience predation risk.
The results revealed no specific pattern of cumulative effects of predation risk; however, there were sex-specific and stage-specific consequences of early risk exposure. Male mosquitoes were adversely affected, whereas females showed no immediate costs. The non-feeding pupal stage was less effective at managing trade-offs than the larval stage, with higher fitness costs observed when predation risk was experienced during the pupal stage. Together, these findings highlight the stage- and sex-specific nature of trade-offs in holometabolous insects.
Contributions and implications
My thesis makes several critical contributions to understanding the life-history evolution of complex life cycles. First, it provides evidence of behavioural carryover in the pupal stage of a holometabolous insect, demonstrating that early life experiences can influence behaviour even after metamorphosis. Second, it highlights the pupal stage’s ability to modulate behaviour based on ecological payoffs. Finally, it offers a comprehensive analysis of multistage trade-offs, revealing that the timing of predation risk exposure impacts fitness. By focussing on pupa, a critical yet understudied stage, this thesis expands the knowledge of life-history trade-offs and evolutionary processes in complex life cycles. The findings underscore the importance of considering the entire life cycle when studying the evolutionary ecology of organisms. | en_US |
