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Background  Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these cases involve loss-of-function mutations in one or more trait-specific genes. However, in parasitoid insects the evolutionary loss of a metabolic trait is not associated with gene decay. Parasitoids have lost the ability to convert dietary sugars into fatty acids. Earlier research suggests that lack of lipogenesis in the parasitoid wasp  Nasonia vitripennis  is caused by changes in gene regulation.    Results  We compared transcriptomic responses to sugar-feeding in the non-lipogenic parasitoid species  Nasonia vitripennis  and the lipogenic  Drosophila melanogaster . Both species adjusted their metabolism within 4 hours after sugar-feeding, but there were sharp differences between the expression profiles of the two species, especially in the carbohydrate and lipid metabolic pathways. Several genes coding for key enzymes in acetyl-CoA metabolism, such as  malonyl-CoA decarboxylase  ( mcd ) and  HMG-CoA synthase  ( hmgs ) differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network-based analysis showed connectivity of genes to be negatively correlated to the fold change of gene expression. Furthermore, genes involved in the fatty acid metabolic pathway were more connected than the set of genes of all metabolic pathways combined.    Conclusion  High connectivity of lipogenesis genes is indicative of pleiotropic effects and could explain the absence of gene degradation. We conclude that modification of expression levels of only a few little-connected genes, such as  mcd , is sufficient to enable complete loss of lipogenesis in  N. vitripennis .    Electronic supplementary material  The online version of this article (10.1186/s12864-019-5673-6) contains supplementary material, which is available to authorized users.

Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids