Assessment of phenotypic plasticity for lipogenesis in Leptopilina heterotoma populations as an alternative hypothesis to loss and re-acquisition of fat synthesis in parasitic wasps

There are many documented examples of cases of evolutionary adaptation loss and regain, known as reverse evolution. These cases are in contradiction with Dollo’s law, which states that the evolutionary loss of a complex trait is irreversible. Loss of lipogenesis in parasitic wasps is one illustration of reverse evolution. Although lipid synthesis is usually highly conserved across living organisms and throughout time, the intrinsic host-parasitoid relationship that characterizes parasitic wasps is thought to have led to an adaptive loss for the ability to synthesize lipids. Hymenopteran parasitoids are indeed very efficient in manipulating their host fat content for their own benefit, so that lipogenesis, which is costly, has become redundant. In addition, the re-acquisition of lipid synthesis is mainly found in parasitic wasps that are host generalists and might thus not be as efficient in manipulating their host fat content. Interestingly, the species Leptopilina heterotoma revealed variation in its ability to synthesize lipids, while no genetic heterogeneity was found to explain these fluctuations. This intraspecific variation thus suggested lipogenesis could in fact be plastic. Lipogenesis would be switched on in fat-poor environments and switched off when fat-rich environmental conditions are met. Stable isotope tracing was used to assess this adaptive plasticity hypothesis, where the environmental cue was assimilated to two different host species, known to differ in their fat content: Drosophila melanogaster and Drosophila simulans. Lipid extraction and GC-MS analyses where then performed to assess lipid incorporation of the isotope, deuterium, between the two groups of individuals, either fat-rich (D. melanogaster) or fat-poor (D. simulans) raised. A familial design in which different families were created was set, which insured daughters of a same lineage would share 75% of their genome. It was expected that individuals raised on D. simulans would trigger lipogenesis, and that percent incorporation would be higher in samples issued from fat-poor hosts. Although not statistically significant, a substantial difference was found between the two host groups, with higher percent average incorporation found in fat-poor host compared to fat-rich host. Moreover, fluctuations in the reaction norms as well as in the amount of percent incorporation on D. melanogaster between the population groups and family groups further suggest that there would be genetic variation for lipogenesis plasticity, which could thus either be favored or selected against. In conclusion, the results presented here tend to confirm the plasticity hypothesis, which would also apply to other cases of loss and regain of lipid synthesis in parasitic wasps. Additionally, further confirmation of plasticity hypothesis would be of great interest and have major impact, as other well-known cases of reverse evolution could in fact hide adaptive environmental plasticity.