MicroRNAs Associated with Caste Determination and Differentiation in a Primitively Eusocial Insect

David H Collins,Vincent Moulton,Matthew Beckers,Irina Mohorianu,Andrew F G Bourke,Tamas Dalmay

doi:10.1038/srep45674

David H Collins, Vincent Moulton + Show 4 more

Open Access

https://doi.org/10.1038/srep45674

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Abstract

In eusocial Hymenoptera (ants, bees and wasps), queen and worker adult castes typically arise via environmental influences. A fundamental challenge is to understand how a single genome can thereby produce alternative phenotypes. A powerful approach is to compare the molecular basis of caste determination and differentiation along the evolutionary trajectory between primitively and advanced eusocial species, which have, respectively, relatively undifferentiated and strongly differentiated adult castes. In the advanced eusocial honeybee, Apis mellifera, studies suggest that microRNAs (miRNAs) play an important role in the molecular basis of caste determination and differentiation. To investigate how miRNAs affect caste in eusocial evolution, we used deep sequencing and Northern blots to isolate caste-associated miRNAs in the primitively eusocial bumblebee Bombus terrestris. We found that the miRNAs Bte-miR-6001-5p and -3p are more highly expressed in queen- than in worker-destined late-instar larvae. These are the first caste-associated miRNAs from outside advanced eusocial Hymenoptera, so providing evidence for caste-associated miRNAs occurring relatively early in eusocial evolution. Moreover, we found little evidence that miRNAs previously shown to be associated with caste in A. mellifera were differentially expressed across caste pathways in B. terrestris, suggesting that, in eusocial evolution, the caste-associated role of individual miRNAs is not conserved.

Highlights

Eusocial insects are characterized by exhibiting castes, with the queen caste being specialized for reproduction and the worker caste being specialized for non-reproductive, colony tasks[1,2,3]
In eusocial Hymenoptera, the potential role of miRNAs in caste development has been studied in the honeybee, Apis mellifera, where miRNAs have been shown to be differentially expressed in queen- and worker-destined larvae and pupae[20,21,22] and experimentally implicated in caste determination[23]
Each phenotype was sequenced in four biological replicates, comprising paired but separate pools of early- and late-instar larvae within each caste pathway from each of eight separate colonies, yielding 16 samples in total

Summary

Introduction

Eusocial insects are characterized by exhibiting castes, with the queen caste being specialized for reproduction and the worker caste being specialized for non-reproductive, colony tasks[1,2,3]. To address the molecular basis of caste development, several previous studies have used genomic approaches such as high-throughput sequencing to profile the genes associated with caste determination and differentiation in a range of eusocial Hymenoptera[6,7,8,9,10,11,12,13,14]. Bombus represents the closest extant model for the primitively eusocial common ancestor with Apis, albeit one that, since the split, will have undergone independent evolution towards its own form of eusociality For these reasons, B. terrestris makes an excellent system in which to investigate the molecular basis of queen-worker caste differentiation and determination, including the role of miRNAs, in the evolutionary trajectory between primitive and advanced eusociality. Worker-destined larvae lose totipotency and cannot change to the queen pathway once they have passed the second instar without a JH peak, i.e. if they have passed through the sensitive phase in the queen’s presence[28]

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