The Making of a Queen: TOR Pathway Is a Key Player in Diphenic Caste Development

Avani Patel,M Kim Fondrk,Osman Kaftanoglu,Christine Emore,Katy Frederick,Gro V Amdam,Greg Hunt,Pawel Michalak

doi:10.1371/journal.pone.0000509

Abstract

BackgroundHoney bees (Apis mellifera) provide a principal example of diphenic development. Excess feeding of female larvae results in queens (large reproductives). Moderate diet yields workers (small helpers). The signaling pathway that links provisioning to female developmental fate is not understood, yet we reasoned that it could include TOR (target of rapamycin), a nutrient- and energy-sensing kinase that controls organismal growth.Methodology/Principal FindingsHere, the role of Apis mellifera TOR (amTOR) in caste determination is examined by rapamycin/FK506 pharmacology and RNA interference (RNAi) gene knockdown. We show that in queen-destined larvae, the TOR inhibitor rapamycin induces the development of worker characters that are blocked by the antagonist FK506. Further, queen fate is associated with elevated activity of the Apis mellifera TOR encoding gene, amTOR, and amTOR gene knockdown blocks queen fate and results in individuals with worker morphology.Conclusions/SignificanceA much-studied insect dimorphism, thereby, can be governed by the TOR pathway. Our results present the first evidence for a role of TOR in diphenic development, and suggest that adoption of this ancestral nutrient-sensing cascade is one evolutionary pathway for morphological caste differentiation in social insects.

Highlights

TOR is the central component of a conserved eukaryotic signaling pathway that regulates cell and organismal growth in response to nutrient status [1,2]
We explored if the critical decision-point of caste determination (3rd larval instar) was characterized by variation in Apis mellifera TOR (amTOR) expression that correlated with developmental fate
Our findings show that amTOR can govern the suites of morphological characters that differentiate honey bee queens and workers

Summary

Introduction

TOR is the central component of a conserved eukaryotic signaling pathway that regulates cell and organismal growth in response to nutrient status [1,2]. Suppression of the Drosophila TOR pathway results in prolonged pre-adult development and reduces larval and adult body sizes [2] These signatures of experimental variation in TOR signaling strikingly resemble the naturally occurring diphenism of the highly eusocial honey bee, where two alternative female phenotypes – the reproductive queen caste and the facultatively sterile worker caste – differentiate through social manipulation of larval nutrient status [5]. Queen-destined individuals, which receive a rich diet of royal jelly as larvae, are from the 3rd instar characterized by accelerated larval growth, upregulation of larval ribosomal and metabolic gene expression, rapid pre-adult development and large body sizes [5,6,7]. Our results present the first evidence for a role of TOR in diphenic development, and suggest that adoption of this ancestral nutrient-sensing cascade is one evolutionary pathway for morphological caste differentiation in social insects

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