Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta).

Chloe Hawkings,Cecilia Tamborindeguy

doi:10.7717/peerj.4875

Abstract

Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potentially fertile nurses, and to other ant species that lay trophic eggs, S. invicta workers completely lack ovaries or the ability to lay eggs. This provides a unique model to investigate whether Vg duplication in S. invicta was followed by subfunctionalization to acquire non-reproductive functions and whether Vg was co-opted to regulate behavior within the worker caste. To investigate these questions, we compared the expression patterns of S. invicta Vg genes among workers from different morphological subcastes or performing different tasks. RT-qPCRs revealed higher relative expression of Vg1 in major workers compared to both medium and minor workers, and of Vg2 in major workers when compared to minor workers. Relative expression of Vg1 was also higher in carbohydrate foragers when compared to nurses and protein foragers. By contrast, the level of expression of Vg2, Vg3, and Vg4 were not significantly different among the workers performing the specific tasks. Additionally, we analyzed the relationship between the expression of the Vg genes and S-hydroprene, a juvenile hormone analog. No changes in Vg expression were recorded in workers 12 h after application of the analog. Our results suggest that in S. invicta the Vg gene underwent subfunctionalization after duplication to new functions based on the expression bias observed in these data. This may suggest an alternative and still unknown function for Vg in the workers that needs to be investigated further.

Highlights

Division of labor and foraging specialization are a key characteristic of the eusocial insect colony structure
The encoded proteins were 3,312, 1,807, and 1,761 amino acids (AAs) in length, respectively. Further analyses of these proteins revealed that Vg1 encoded a putative signal peptide predicted to be cleaved at position 29, two Vitellogenin N-terminus domains (AAs 34–736 and 1684–2,389), two domains of unknown function (DUF1943) (AAs 770–1,032 and 2,445–2,677), and two von Willebrand factor type D (VWD) domains (AAs 1,428–1,591 and 3,079–3,247) (Fig. 2)
Vg2 is correlated with subcaste size, potentially suggesting a size-biased expression in the workers, in particular in the major workers, which have a higher expression than smaller workers

Summary

Introduction

Division of labor and foraging specialization are a key characteristic of the eusocial insect colony structure. In the honey bee worker caste Vg is involved in royal jelly production (Amdam et al, 2003), age polyethism regulation (Marco Antonio et al, 2008), antioxidant and immunity regulation, and insulin/insulin-like signaling which controls growth, aging, and reproduction (Amdam et al, 2006; Keller & Jemielity, 2006). This relationship between Vg and task has been recognized across species of ants (Corona et al, 2013; Graff et al, 2007; Hartmann & Heinze, 2003; Martinez & Wheeler, 1991)

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