Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic wasps.

Authors: VISSER, BERTANNE - University Of Louvain; Alborn, Hans; RONDEAUX, SUZON - University Of Louvain; HAILLOT, MANON - University Of Louvain; HANCE, THIERRY - University Of Louvain; REBAR, DARREN - Emporia State University; REIDERER, JANA - University Of Groningen; TISO, STEFANO - University Of Groningen; VAN ELDIJK, TIMO - University Of Groningen; WEISSING, FRANZ - University Of Groningen; NIEBERDING, CARLINE - University Of Louvain

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2021
Publication Date: 4/8/2021
Citation: Visser, B.; Alborn, H.T.; Rondeaux, S.; Haillot, M; Hance, T.; Rebar, D.; Reiderer, J.M.; Tiso, S.; Van Eldijk, T.J.; Weissing, F.J.; Nieberding, C.M. 2021. Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic wasps.. Scientific Reports. 11:775. https://doi.org/10.1038/s41598-021-86736-8.
DOI: https://doi.org/10.1038/s41598-021-86736-8

Interpretive Summary: Evolutionary changes have long been considered irreversible, yet recent comparative studies have suggested that certain traits can re-evolve. By utilizing novel labeling incorporation techniques, a scientist at the Chemistry Research Unit, USDA-ARS, CMAVE in Gainesville, FL, in collaboration with a research group at Université Catholique in Brussel, Belgium, investigated lipid synthesis in the parasitic wasp Leptopilina heterotomas. The researchers found that the lipid synthesis, which was thought to have been evolutionally lost and subsequently regained, was actually dependent on environmental conditions of the wasp. Although wasp populations are genetically homogeneous, substantial variation in lipid synthesis plasticity was found among wasp families within populations, indicating that the evolution of lipid synthesis regulation can occur rapidly in response to variation in lipid content. The scientists also found similar phenotypic plasticity in other insect species. These results may form the basis for related research on many beneficial insects, both beneficial and pest, and thus directly relevant for agriculture.

Technical Abstract: Trait loss is pervasive across taxa, leading to the loss of genetic diversity and, in some instances, the extinction of species. Regaining lost traits was long thought impossible, a.k.a. Dollo’s law3, but more cases of reverse phenotypic evolution have accumulated over the years. It has remained unclear, however, how traits lost dozens to millions of years can re-evolve. One such trait is lipid synthesis (“LS” hereafter), a process that is essential for all living organisms. Here, we discovered that LS, which was thought to be lost and repeatedly regained in parasitic wasps (i.e. parasitoids that develop in, and ultimately kill, their arthropod host) is plastic in the wasp Leptopilina heterotoma. LS depends on host lipid content in different field-caught populations, where LS was typically induced on lean fly hosts and completely shut off on fat hosts. Although wasp populations are genetically homogeneous, substantial genetic variation in LS plasticity was found among wasp families within populations, indicating that the evolution of LS regulation can occur rapidly in response to variation in host lipid content. We hypothesized that the apparent evolutionary loss of LS along the evolutionary history of insect parasitoids may in fact be selection on plasticity. As expected, we found functional coding sequences for key genes involved in fatty acid synthesis in the genome of a sister species of L. heterotoma, L. clavipes, as well as the genomes of more distantly related wasp, fly and beetle parasitoids. Our data lead us to propose that selection on plastic expression of LS, rather than loss of LS, explains the maintenance and diversification of parasitic hymenopterans over evolutionary time.