Abstract
The emergence of eusociality (“true sociality”) in several insect lineages represents one of the most successful evolutionary adaptations in the animal kingdom in terms of species richness and global biomass. In contrast to solitary insects, eusocial insects evolved a set of unique behavioral and physiological traits such as reproductive division of labor and cooperative brood care, which likely played a major role in their ecological success. The molecular mechanisms that support the social regulation of behavior in eusocial insects, and their evolution, are mostly unknown. The recent whole-genome sequencing of several eusocial insect species set the stage for deciphering the molecular and genetic bases of eusociality, and the possible evolutionary modifications that led to it. Studies of mRNA expression patterns in the brains of diverse eusocial insect species have indicated that specific social behavioral states of individual workers and queens are often associated with particular tissue-specific transcriptional profiles. Here, we discuss recent findings that highlight the role of non-coding microRNAs (miRNAs) in modulating traits associated with reproductive and behavioral divisions of labor in eusocial insects. We provide bioinformatic and phylogenetic data, which suggest that some Hymenoptera-specific miRNA may have contributed to the evolution of traits important for the evolution of eusociality in this group.
Highlights
Most insect species are solitary, and behavioral interactions with conspecifics are primarily restricted to reproductive behaviors such as male–female courtship and male–male competition
In honey bees is not known, previous reports indicate that miR-124 is an evolutionary conserved, brain-enriched miRNA that plays a role in neural development and plasticity in invertebrates, birds, and mammals (Cao et al, 2007; Makeyev et al, 2007; Rajasethupathy et al, 2009), and in the development and function of the peripheral sensory system in C. elegans (Clark et al, 2010). miR-275 is conserved across insects, and has been implicated in the regulation of egg laying behavior in Aedes aegypti (Bryant et al, 2010)
We propose that the molecular evolution of specific miRNAs could have contributed to the phenotypic evolution of eusociality. We propose that these miRNAs may have contributed to the emergence of eusociality by either introducing new regulatory nodes to ancestral behavioral genetic networks, and/or by supporting novel behavioral genetic networks
Summary
Most insect species are solitary, and behavioral interactions with conspecifics are primarily restricted to reproductive behaviors such as male–female courtship and male–male competition. Queen-destined larvae that were fed with royal jelly supplemented with the worker-enriched miRNA ame-miR-184 developed some workerlike morphologies (e.g., smaller body and shorter wings) This remarkable finding suggests that in honey bees, the consumption of exogenous miRNAs could play an important role in the differentiation of totipotent larvae into either sterile workers or reproductive queens. In this context, the conserved role of miR-184 in the regulation of neuroendocrine functions across different animal taxa (Morita et al, 2013) is alluring. In honey bees is not known, previous reports indicate that miR-124 is an evolutionary conserved, brain-enriched miRNA that plays a role in neural development and plasticity in invertebrates, birds, and mammals (Cao et al, 2007; Makeyev et al, 2007; Rajasethupathy et al, 2009), and in the development and function of the peripheral sensory system in C. elegans (Clark et al, 2010). miR-275 is conserved across insects, and has been implicated in the regulation of egg laying behavior in Aedes aegypti (Bryant et al, 2010). Wu et al (2014) speculated that the upregulation of ame-miR-124 miRNA in virgin queens might be related to the modulation of sensory and/or other neuronal functions associated with mating behaviors, while the increased expression of ame-miR-275 in mated queens might be important for the newly mated queens to initiate egg-laying behavior
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