Brain gene expression analyses in virgin and mated queens of fire ants reveal mating-independent and socially regulated changes.

Travis L Calkins,Patricia V Pietrantonio,Arinder K Arora,Chloe Hawkings,Mei-Er Chen,Cecilia Tamborindeguy

doi:10.1002/ece3.3976

Abstract

Transcriptomes of dissected brains from virgin alate and dealate mated queens from polygyne fire ants (Solenopsis invicta) were analyzed and compared. Thirteen genes were upregulated in mated queen brain, and nine were downregulated. While many of the regulated genes were either uncharacterized or noncoding RNAs, those annotated genes included two hexamerin proteins, astakine neuropeptide, serine proteases, and serine protease inhibitors. We found that for select differentially expressed genes in the brain, changes in gene expression were most likely driven by the changes in physiological state (i.e., age, nutritional status, or dominance rank) or in social environment (released from influence of primer pheromone). This was concluded because virgins that dealated after being separated from mated queens showed similar patterns of gene expression in the brain as those of mated queens for hexamerin 1, astakine, and XR_850909. Abaecin (XR_850725), however, appears upregulated only after mating. Therefore, our findings contribute to distinguish how specific gene networks, especially those influenced by queen primer pheromone, are regulated in queen ants. Additionally, to identify brain signaling pathways, we mined the fire ant genome and compiled a list of G‐protein‐coupled receptors (GPCRs). The expression level of GPCRs and other genes in the “genetic toolkit” in the brains of virgin alates and mated dealate queens is reported.

Highlights

The red imported fire ant (Solenopsis invicta Buren) relies on reproductive queens to produce eggs, and completely sterile female workers devoid of ovaries (Khila & Abouheif, 2008) to forage, rear brood, defend the colony, and perform other nest-maintaining tasks.This invasive species has two genetically determined social forms, monogyne, in which colonies have a single mated queen, and polygyne, in which multiple mated queens cooperate (Ascunce et al, 2011)
We aimed to (1) identify differentially expressed genes (DEGs) among these two conditions; (2) compile the currently annotated G-protein-coupled receptors (GPCRs) genes in the fire ant genome (Wurm et al, 2011) and identify those GPCRs transcripts expressed in the fire ant brain that may contribute to relevant signaling networks in queens, as we showed for the sNPF receptor
We investigated whether the level of expression of the validated genes identified as differentially expressed by transcriptome analyses changed in newly mated queens and in virgin queens held in queenright or queenless conditions; (3) we tested the hypothesis that expression of hexamerin-like mRNA in virgin queens is controlled by juvenile hormone (JH) by applying a JH mimic

Summary

Introduction

The red imported fire ant (Solenopsis invicta Buren) relies on reproductive queens to produce eggs, and completely sterile female workers devoid of ovaries (Khila & Abouheif, 2008) to forage, rear brood, defend the colony, and perform other nest-maintaining tasks.This invasive species has two genetically determined social forms, monogyne, in which colonies have a single mated queen, and polygyne, in which multiple mated queens cooperate (Ascunce et al, 2011). The red imported fire ant (Solenopsis invicta Buren) relies on reproductive queens to produce eggs, and completely sterile female workers devoid of ovaries (Khila & Abouheif, 2008) to forage, rear brood, defend the colony, and perform other nest-maintaining tasks. Alate virgin queens shed their wings and their ovaries develop after being experimentally removed from queen pheromonal influences (Fletcher & Blum, 1981, 1983; Vargo, 1999), coinciding with global changes in gene expression as reported with queen whole bodies (Wurm, Wang, & Keller, 2010). In this scenario, when several alate queens are grouped, those that dealate first exhibit dominance, preventing the remaining alates from dealation (Fletcher, Cherix, & Blum, 1983)

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