Gene regulatory mechanisms underlying the evolutionary loss of a polygenic trait

Abstract

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 involve loss-of-function mutations in one or more trait-specific genes. Parasitoid insects are fatty acid auxotrophs: they lost the ability to convert dietary sugars into fatty acids, a trait that is ubiquitous among non-parasitoid animals and is enabled by a highly conserved set of genes. Earlier research suggests that lack of lipogenesis is caused by changes in gene regulation, rather than gene decay. We compared transcriptome-wide responses to sugar-feeding in the non-lipogenic parasitoid species Nasonia vitripennis and the lipogenic Drosophila melanogaster. Both species adjusted their metabolism within four hours after feeding, but there was little overlap at the gene level between the responses of the two species. Even at the pathway-level, there were sharp differences between the expression profiles of the two species, especially in 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 differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network analysis indicates most genes involved in these pathways to be highly connected, which suggest they have pleiotropic effects and could explain the absence of gene degradation. Our results indicate that modification of expression levels of only a few non-connected genes, such as MCD, is sufficient to enable complete loss of lipogenesis in N. vitripennis.