Abstract
The major environmental determinants of honeybee caste development come from larval nutrients: royal jelly stimulates the differentiation of larvae into queens, whereas beebread leads to worker bee fate. However, these determinants are not fully characterized. Here we report that plant RNAs, particularly miRNAs, which are more enriched in beebread than in royal jelly, delay development and decrease body and ovary size in honeybees, thereby preventing larval differentiation into queens and inducing development into worker bees. Mechanistic studies reveal that amTOR, a stimulatory gene in caste differentiation, is the direct target of miR162a. Interestingly, the same effect also exists in non-social Drosophila. When such plant RNAs and miRNAs are fed to Drosophila larvae, they cause extended developmental times and reductions in body weight and length, ovary size and fecundity. This study identifies an uncharacterized function of plant miRNAs that fine-tunes honeybee caste development, offering hints for understanding cross-kingdom interaction and co-evolution.
Highlights
Caste development in social insects represents a major transition from one level of organization to another in evolution and is believed to be central to the ecological success of social insects [1]
Since miRNAs are transmitted between species of different kingdoms and can contribute to the phenotype regulation, this new model of horizontal miRNA transfer may open up a new avenue to further study the molecular mechanisms underlying cross-kingdom interaction and co-evolution
Female honeybees develop into two castes, queens and workers, which differ in morphology, physiology and social function [1, 2]
Summary
Caste development in social insects represents a major transition from one level of organization to another in evolution and is believed to be central to the ecological success of social insects [1]. The queens are reproductive, have a larger body size, develop faster and live longer, whereas workers are characterized by the opposite traits and are mostly sterile helpers that nourish larvae and collect food [3] This dimorphism is not a consequence of genetic differences but is mainly determined by larval feeding: female larvae receiving a rich diet of royal jelly develop into queens, whereas a less sophisticated diet named “beebread” leads to the worker bee fate [4, 5]. It is still not fully understood how different diets modify the developmental trajectory of honeybees to such a thorough extent. We investigated a largely overlooked component of larval food, microRNA (miRNA), and examined its effect on caste development
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