Niche realisation processes in a holometabolous insect. Effects of starvation and pharmacophagy in the turnip sawfly

The turnip sawfly, Athalia rosae, a holometabolous insect with distinct larval and adult ecology, provides an exemplary model for investigating the complex mechanisms of niche realisation processes. As individuals navigate a multifaceted environment, their phenotypes are shaped by a dynamic interplay between adaptation to environmental constraints, and actively choosing and modifying their immediate surroundings. This thesis explores how individuals of this species realise their niche in relation to two specific mediators: starvation and pharmacophagy. Starvation and pharmacophagy are two particularly important factors across the life cycle of A. rosae. Starvation is the absence or limitation of nutritional resources and can fundamentally affect individual life-history, physiology, and behaviour. Pharmacophagy represents the active uptake of plant specialised metabolites that are not directly related to nutritional requirements but provide benefits such as enhanced defence against predators or benefits in mating. Nutritional stress, specifically starvation, represents a significant environmental pressure that elicits profound plastic responses in A. rosae. The impact of this stressor is not uniform across the insect's lifespan. Its effects are contingent upon the developmental stage at which it is experienced. In Chapter 2, we found that starvation during the larval stage primarily impacts developmental life-history traits. For both sexes, this early-life stress leads to a significantly prolonged development time. Females, however, appear more sensitive in terms of biomass accumulation, emerging with a significantly lower initial adult body mass compared to their non-starved conspecifics. In contrast, males demonstrate a higher capacity to compensate for poor larval conditions, maintaining an initial adult body mass comparable to that of non-starved individuals. Starvation during the adult stage led to effects on metabolic traits. This nutritional stress in the adult stage predominantly affects energy reserves, leading to the depletion of both carbohydrate and lipid stores. This effect is particularly pronounced in males subjected to either adult stage starvation or repeated stress during both larval and adult stage. However, adult lifespan and general activity levels remain largely unaffected by starvation. This demonstrates that individual sensitivity to nutritional stress is highly life stage- and sex-specific with dependence on the biological trait in consideration. In addition to nutritional limitation, the non-nutritional acquisition of plant specialised metabolites is an important mediator in niche realisation processes of A. rosae. This phenomenon, known as pharmacophagy, involves adults seeking out and consuming specialised neo-clerodane diterpenoids (clerodanoids) from the leaves of the bugleweed, Ajuga reptans, through a characteristic licking behaviour, unrelated to nutrition. In Chapter 3, we found that consumed clerodanoids are metabolised into two distinct clerodanoid-derived compounds with masses of 482 and 484 Da. These modified compounds are not only stored internally within the thorax and abdomen, but are also localised on the insect's body surface. Interestingly, A. rosae larvae, which do not naturally encounter A. reptans, are also able to metabolise these compounds, a finding that may be connected to an ancestral evolutionary link to Lamiales host plants. In Chapter 4, we focused on perception, uptake mechanisms and cuticular hydrocarbons in relation to pharmacophagy. Sawflies seem not to detect clerodanoids via long-distance olfaction but rather perceive the relevant compounds at close distances, pointing to a contact stimulus that triggers the licking response. This close-distance perception is the mechanism enabling kleptopharmacophagy, the direct acquisition of these defensive compounds by licking the surface of conspecifics that have previously been exposed to the plant. While this pharmacophagous activity is central to the sawfly's mating and defence strategies, it does not alter the composition of their cuticular hydrocarbons. (CHCs). The CHC profile itself exhibits a quantitative sexual dimorphism, which is driven primarily by the lower abundance of three key compounds in females compared to males, but the CHC profile seems to be unaffected by clerodanoid acquisition. In conclusion, our studies collectively provide new insights into the individualised niches of A. rosae, and the effects of starvation and pharmacophagy. These distinct factors are two examples of mediators that generate individual-level variation, which vary in relation to life stage, sex, and the biological trait under consideration. Collectively, this thesis highlights the intricate interplay between nutrition, behaviour, and chemical communication in affecting niche realisation processes of A. rosae. By combining chemical analyses and behavioural assays we could disentangle effects of starvation and pharmacophagy. Our findings contribute to the understanding of individual needs and facilitate a broader understanding of how insects adapt to changing environments.