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Ecological conditions underlying the lack of lipid synthesis in parasitic insects

Final Report Summary - ECOLOGY&LIPOGENESIS (Ecological conditions underlying the lack of lipid synthesis in parasitic insects)

The main goal of this Marie Curie project was to unravel the underlying causes and consequences of atypical metabolism, i.e. the inability to make fat, in parasitic wasps. Our project has clarified key aspects of the nutritional ecology of the model systems employed, including lipogenic abilities and lifetime nutrient dynamics. Our work has revealed that 1) maternal nutrient provisioning affects offspring metabolism, 2) parasitoid larvae lack lipid synthesis, and 3) populations vary in the ability for lipid synthesis. More information can be obtained from the project website:

1) Maternal nutrient provisioning affects offspring metabolism
The internal physiological state of a mother can have major consequences for her fitness and that of her offspring. In collaboration with Prof. Emmanuel Desouhant (Lyon Univ, FR), we have shown that transgenerational effects in the parasitic wasp E. vuilleti become apparent when old mothers provision their eggs with less protein, sugar and lipid. Feeding from a host after hatching allows the offspring of old mothers to overcome initial shortages in sugars and lipids, but adult offspring of old mothers emerged with lower amounts of protein and glycogen. Reduced egg provisioning by old mothers had adverse consequences for the nutrient composition of adult female offspring, despite larval feeding from a high-quality host. Lower resource availability in adult female offspring of old mothers may thus lead to grandparental effects that affect behavioral decisions, life histories and performance of future generations. Studying the physiology of transgenerational effects advances our understanding of the mechanisms at work in shaping non-genetic individual variation, life histories and population dynamics. This work has led to one publication, which is currently submitted.

2) Lipid synthesis in parasitoid larvae
Symbiotic interactions can lead to the loss of essential traits, for instance in parasitic wasps (i.e. parasitoids) that feed from a host during development and that have lost the ability to synthesize lipids. A key hypothesis as to the evolutionary loss of lipid synthesis is that this trait was lost as a consequence of negative selection on larvae. Costly lipid synthesis could be avoided, but only in larvae that can readily take over lipids from their host. It has remained unclear, however, whether parasitoid larvae synthesize lipids. Measuring lipid synthesis in adult parasitoids is straightforward, but the close association between larvae and their hosts complicates the separation of host and parasitoid metabolism. In collaboration with Hans Alborn (USDA Lead Scientist; Chemistry Group; Gainesville, Florida, USA), we developed a novel method to determine larval lipid synthesis by separating parasitoid from host metabolism. This method enabled us to detach early developing parasitoids from their host to topically apply the stable isotope deuterium. Following topic application, we traced the fate of this stable isotope into the fatty acid fraction at the end of larval development to determine lipogenic ability of larvae. Similar to adults, parasitoid larvae do not synthesize lipids, revealing that lipogenic strategies are similar across life stages and that lipid synthesis was indeed lost as a consequence of selection acting on larvae. This work has led to one publication, which is currently being prepared for submission.

3) Populations vary in the ability for lipid synthesis
It has been known for several years that the majority of parasitoids do not synthesize fat, but that some species are still capable of lipid synthesis. Moreover, reports suggested that for one parasitoid species lipogenic ability may vary at the population-level. Such variability within species opens up numerous new avenues for research into the evolution of lipid synthesis; hence I set out to find populations that varied in lipogenic ability.
We started by collecting parasitoids from the field at 12 different geographical locations in 4 countries. We then successfully set up 9 laboratory cultures corresponding to 9 distinct geographical locations and maintained parasitoids in large numbers to develop several methods for determining lipogenic ability (Fig. 1).
The first task after collection of these populations was to determine that all populations belonged to the same species. Using 3 different methods, i.e. inter-population mating trials (performed by my MSc student), morphological verification (in collaboration with Prof Goran Nordlander, SE) and genomics (COI analysis performed by Dr Simon Dupont at the host institute), these methods have unequivocally shown that our populations all belong to the same species.
Using gravimetric analysis we then determined lipogenic ability for each of the populations. we have now collected data comparing lipid levels of female parasitoids at emergence and after 10 days of feeding on honey. These data showed that 2 out of 9 population lack lipogenesis (lipid levels either remain stable or decrease), whilst the other populations actively synthesize lipids (increasing lipid levels; Fig. 1; Fig. 2).
The next step is to determine the physiological and life history consequences of variation in lipogenic ability between populations. We can now also look into the mechanisms underlying populational variability in lipid synthesis and estimate how quickly populations can switch strategies under different environmental settings. These questions will be addressed in my future research program for which new funding has been obtained.