Data from: Making a queen: an epigenetic analysis of the robustness of the honey bee (Apis mellifera) queen developmental pathway

Specialized castes are considered a key reason for the evolutionary and
ecological success of the social insect lifestyle. The most essential
caste distinction is between the fertile queen and the sterile workers.
Honeybee (Apis mellifera) workers and queens are not genetically distinct,
rather these different phenotypes are the result of epigenetically
regulated divergent developmental pathways. This is an important
phenomenon in understanding the evolution of social insect societies.
Here, we studied the genomic regulation of the worker and queen
developmental pathways, and the robustness of the pathways by
transplanting eggs or young larvae to queen cells. Queens could be
successfully reared from worker larvae transplanted up to 3 days age, but
queens reared from older worker larvae had decreased queen body size and
weight compared with queens from transplanted eggs. Gene expression
analysis showed that queens raised from worker larvae differed from queens
raised from eggs in the expression of genes involved in the immune system,
caste differentiation, body development and longevity. DNA methylation
levels were also higher in 3-day-old queen larvae raised from worker
larvae compared with that raised from transplanted eggs identifying a
possible mechanism stabilizing the two developmental paths. We propose
that environmental (nutrition and space) changes induced by the commercial
rearing practice result in a suboptimal queen phenotype via epigenetic
processes, which may potentially contribute to the evolution of
queen–worker dimorphism. This also has potentially contributed to the
global increase in honeybee colony failure rates.

特化品级（caste）被认为是社会性昆虫（social insect）生活方式在演化与生态层面取得成功的核心原因。其中最关键的品级分化，存在于可育蜂王与不育工蜂之间。西方蜜蜂（Apis mellifera）的工蜂与蜂王并无遗传差异，二者迥异的表型实为表观遗传调控的差异化发育通路所造就。这一现象对于解析社会性昆虫社会的演化机制具有重要学术价值。本研究围绕工蜂与蜂王发育通路的基因组调控机制，以及通过将卵或幼幼虫移植至王台以验证该通路的稳定性展开。实验结果显示，日龄不超过3天的工蜂幼虫可被成功诱导发育为蜂王，但由日龄更大的工蜂幼虫培育出的蜂王，其体型与体重均低于由移植卵培育的蜂王。基因表达分析表明，由工蜂幼虫培育的蜂王与由卵培育的蜂王，在免疫系统、品级分化、躯体发育及寿命相关基因的表达模式上存在显著差异。相较于由移植卵培育的蜂王幼虫，由工蜂幼虫培育的3日龄蜂王幼虫的DNA甲基化水平更高，这揭示了稳定两种发育通路的潜在表观遗传机制。我们提出，商业化育王实践所带来的环境（营养与空间）变化，可通过表观遗传过程催生次优的蜂王表型，这或可推动蜂王-工蜂二态性的演化，同时也可能与全球范围内蜜蜂蜂群损失率的攀升存在关联。