Data from: Transcriptional markers of sub-optimal nutrition in developing Apis mellifera nurse workers

Background: Honey bees (Apis mellifera) contribute substantially to the worldwide economy and ecosystem health as pollinators. Pollen is essential to the bee’s diet, providing protein, lipids, and micronutrients. The dramatic shifts in physiology, anatomy, and behavior that accompany normal worker development are highly plastic and recent work demonstrates that development, particularly the transition from nurse to foraging roles, is greatly impacted by diet. However, the role that diet plays in the developmental transition of newly eclosed bees to nurse workers is poorly understood. To further understand honey bee nutrition and the role of diet in nurse development, we used a high-throughput screen of the transcriptome of 3 day and 8 day old worker bees fed either honey and stored pollen (rich diet) or honey alone (poor diet) within the hive. We employed a three factor (age, diet, age x diet) analysis of the transcriptome to determine whether diet affected nurse worker physiology and whether poor diet altered the developmental processes normally associated with aging. Results: Substantial changes in gene expression occurred due to starvation. Diet-induced changes in gene transcription occurring in younger bees were largely a subset of those occurring in older bees, but certain signatures of starvation were only evident 8 day old workers. Of the 18,542 annotated genes in the A. mellifera genome, 0.7% (126 genes) exhibited differential expression due to poor diet at 3d of age compared with 81% (15,001 genes) that differed due to poor diet at 8d of age. Of the genes that were differentially expressed in young or old pollen deprived bees, poor diet caused more frequent down-regulation of gene expression in younger bees compared to older bees. In addition, the age-related physiological changes that accompanied early adult development differed due to the diet these young adult bees were fed. More frequent down-regulation of gene expression was observed in developing bees fed a poor diet compared to an adequate diet. Functional analyses also show that the physiological and developmental processes occurring in well-fed bees are vastly different than those occurring in pollen deprived bees. These data support the hypothesis that poor diet causes normal age-related development to go awry. Conclusion: Poor nutrition has major consequences for the expression of genes underlying the physiology and age-related development of nurse worker bees. More work is certainly needed to fully understand the consequences of starvation and the complex biology of nutrition and development in this system, but the genes identified in the present study provide a starting point for understanding the consequences of poor diet and for mitigating the economic costs of colony starvation.

背景：西方蜜蜂（Apis mellifera）作为传粉媒介，对全球经济与生态健康贡献卓著。花粉是蜜蜂日粮的必需组分，可为其提供蛋白质、脂质与微量营养素。正常工蜂发育过程中伴随的生理、解剖与行为剧烈变化具有高度可塑性，近期研究表明，发育进程——尤其是从保育蜂到采集蜂的角色转变——会受到日粮的显著调控。然而，日粮在新羽化蜜蜂向保育工蜂发育转变过程中所发挥的作用，目前仍有待深入解析。为进一步阐明蜜蜂营养机制以及日粮在保育蜂发育中的作用，本研究对蜂箱内分别饲喂蜂蜜+贮藏花粉（富日粮）与仅饲喂蜂蜜（贫日粮）的3日龄与8日龄工蜂的转录组（transcriptome）开展了高通量筛选（high-throughput screen）。我们采用三因素（年龄、日粮、年龄×日粮）转录组分析方案，以明确日粮是否会影响保育工蜂的生理状态，以及贫日粮是否会改变与衰老相关的正常发育进程。
结果：饥饿可引发显著的基因表达变化。幼蜂中由日粮差异诱导的转录变化，在很大程度上是老龄蜂中此类变化的子集，但部分饥饿相关的转录特征仅在8日龄工蜂中得以显现。西方蜜蜂基因组（genome）中共注释得到18542个基因，其中3日龄时因贫日粮出现差异表达（differential expression）的基因占比0.7%（共126个），而8日龄时该比例高达81%（共15001个）。在缺粉处理的幼蜂或老龄蜂中出现差异表达的基因里，幼蜂体内由贫日粮导致的基因表达下调频率显著高于老龄蜂。此外，伴随成虫早期发育的年龄相关生理变化，因幼蜂所饲喂的日粮不同而存在显著差异。与饲喂充足日粮的发育蜂相比，饲喂贫日粮的发育蜂中基因表达下调的频率更高。功能富集分析显示，饲喂充足日粮的蜜蜂与缺粉蜜蜂所涉及的生理与发育过程存在显著差异。上述数据支持“贫日粮会扰乱正常的年龄相关发育进程”这一研究假说。
结论：营养不良会对保育工蜂生理及年龄相关发育相关基因的表达产生重大影响。尽管要完全阐明饥饿效应以及该系统中营养与发育的复杂生物学机制仍需开展更多研究，但本研究鉴定得到的差异表达基因可为理解贫日粮的影响、缓解蜂群饥饿带来的经济损失提供重要的研究起点。