Department of Ecological Sciences, Section Animal Ecology, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
BMC Genomics. 2019 Apr 23;20(1):309. doi: 10.1186/s12864-019-5673-6.
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.
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.
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.
性状丧失是进化中普遍存在的现象，但只有少数情况下确定了其潜在的分子原因。这些情况大多数涉及一个或多个特定性状基因的功能丧失突变。然而，在寄生性昆虫中，代谢性状的进化丧失与基因衰减无关。寄生蜂失去了将膳食糖转化为脂肪酸的能力。早期的研究表明，寄生蜂 Nasonia vitripennis 中脂生成缺乏是由于基因调控的变化所致。
我们比较了非脂生性寄生种 Nasonia vitripennis 和脂生性果蝇 Drosophila melanogaster 对糖喂养的转录组反应。这两个物种在糖喂养后 4 小时内都调整了其代谢，但两个物种的表达谱存在明显差异，尤其是在碳水化合物和脂质代谢途径中。编码乙酰辅酶 A 代谢关键酶的几个基因，如丙二酰辅酶 A 脱羧酶（mcd）和 HMG-CoA 合酶（hmgs），在两个物种中的表达存在差异。它们的共同作用可能阻止了寄生物种的脂生成。基于网络的分析表明，基因的连通性与基因表达的倍数变化呈负相关。此外，参与脂肪酸代谢途径的基因比所有代谢途径的基因集合更具连通性。
脂生成基因的高连通性表明存在多效性效应，这可以解释基因衰减的缺失。我们得出结论，仅少数几个连通性较低的基因（如 mcd）的表达水平的修饰就足以使 N. vitripennis 完全丧失脂生成能力。
