Many parasitoids lack adult fat accumulation, despite fatty acid synthesis: A discussion of concepts and considerations for future research

Authors: VISSER, BERTANNE - University Of Liege; LE LANN, CECILE - University Of Rennes; NIEBERDING, CAROLINE - University Of Louvain; LAMMERS, MARK - Muenster University; HAHN, DANIEL - University Of Florida; Alborn, Hans; ENRIQUEZ, THOMAS - University Of Liege; SCHEIFLER, MATHILDE - University Of Liege; HARVEY, JEFFREY - Netherlands Institute Of Ecology; ELLERS, JACINTHA - University Of Amsterdam

Submitted to: Current Opinion in Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2023
Publication Date: 4/10/2023
Citation: Visser, B., Le Lann, C., Nieberding, C.M., Lammers, M., Hahn, D.A., Alborn, H.T., Enriquez, T., Scheifler, M., Harvey, J.A., Ellers, J. 2023. Many parasitoids lack adult fat accumulation, despite fatty acid synthesis: A discussion of concepts and considerations for future research. Current Opinion in Insect Science. 3:100055. https://doi.org/10.1016/j.cris.2023.100055.
DOI: https://doi.org/10.1016/j.cris.2023.100055

Interpretive Summary: In agricultural systems there exists some insects that use other insects as hosts for their eggs. These are known as insect parasitoids and have become important agents for the biological control of insect pests. Lipid (e.g., fatty acids among other non-polar molecules) reserves are a major energy source and play a key role in survival and reproduction of insects; however, in most parasitoid species no adult lipid mass gain takes place, even when nutrients are consumed ad libitum. A USDA-ARS scientist at the Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, in Gainesville FL in collaboration with a multinational team of scientists have previously shown that this lack of lipid mass again (considered a deviating metabolic phenotype) has evolved repeatedly in several parasitoid species. In this paper, we compile a comprehensive list of fat accumulation studies of 35 parasitic wasp species and reflect on new insights and terminology. We clarify the distinct pathways involved in the complex process of the formation of lipids and propose updated, unambiguous terminology, including ‘fatty acid biosynthesis’ and ‘lack of adult fat accumulation’. In addition, we discuss the benefits, drawbacks and complementary information of the main methods available to measure fatty acid biosynthesis and adult fat accumulation. Lastly, we present avenues for future research that combine chemistry, ecology, and evolution into an integrative approach, which is what is now needed to understand the dynamics of fat accumulation in parasitoids.

Technical Abstract: Fat reserves, specifically the accumulation of triacylglycerols, are a major energy source and play a key role for life histories. Fat accumulation is a conserved metabolic pattern across most insects, yet in most parasitoid species adults do not gain fat mass, even when nutrients are readily available and provided ad libitum. This extraordinary physiological phenotype has evolved repeatedly in phylogenetically dispersed parasitoid species. This poses a conundrum because it could lead to significant constraints on energy allocation toward key adult functions such as survival and reproduction. Recent work on the underlying genetic and biochemical mechanisms has spurred a debate on fat accumulation versus fat production, because of incongruent interpretation of results obtained using different methodologies. This debate is in part due to semantics, highlighting the need for a synthetic perspective on fat accumulation that reconciles previous debates and provides new insights and terminology. In this paper, we propose updated, unambiguous terminology for future research in the field, including “fatty acid synthesis” and “lack of adult fat accumulation”, and describe the distinct metabolic pathways involved in the complex process of lipogenesis. We then discuss the benefits and drawbacks of the main methods available to measure fatty acid synthesis and adult fat accumulation. Most importantly, gravimetric/colorimetric and isotope tracking methods give complementary information, provided that they are applied with appropriate controls and interpreted correctly. We also compiled a comprehensive list of fat accumulation studies performed during the last 25 years. We present avenues for future research that combine chemistry, ecology, and evolution into an integrative approach, which we think is needed to understand the dynamics of fat accumulation in parasitoids.