Department of Ecology and Evolutionary Biology, University of Arizona, AZ, USA.
Genome Biol Evol. 2012;4(9):900-16. doi: 10.1093/gbe/evs063. Epub 2012 Jul 19.
Herbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg-adult development time relative to flies reared in glucosinolate knockout (GKO) plants. An analysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. The remaining differentially regulated transcripts also contained a higher proportion of novel genes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.
植食性昆虫是生命中最成功的辐射之一。然而，我们对支持食草进化的过程知之甚少。我们研究了食草在蝇类 Scaptomyza flava 中的进化，其幼虫是十字花科物种的潜叶虫，包括广泛研究的参考植物拟南芥（Arabidopsis）。Scaptomyza flava 在系统发育上嵌套在非单系的果蝇属内，可供 12 种果蝇使用的全基因组序列促进了系统发育分析和 S. flava 转录组的组装。一个时间校准的系统发育表明，Scaptomyza 的潜叶行为在 600 万到 1600 万年前进化而来。饲养实验表明，芥子油苷的生物合成，即芥菜叶中主要的抗食草化学防御化合物，被 S. flava 幼虫的取食上调。与在芥子油苷敲除（GKO）植物中饲养的苍蝇相比，野生型（WT）拟南芥植物中芥子油苷的存在降低了 S. flava 幼虫的体重增加，并延长了卵-成虫的发育时间。对在 WT 与 GKO 植物上饲养的 5 天大的幼虫的基因表达差异分析表明，共有 341 个转录本被幼虫 S. flava 中芥子油苷的摄取差异调节。其中，大约三分之一对应于与饥饿、饮食毒素、热、氧化和衰老相关应激相关的果蝇黑腹果蝇基因的同源物。上调的转录本与未调节的转录本相比，表现出更高的蛋白质进化率。其余差异调节的转录本也比未调节的转录本包含更高比例的新基因。因此，Scaptomyza 向食草的转变似乎与新基因的进化和保守的应激相关基因的共选择有关。
