Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta).

Chloe Hawkings,Travis L Calkins,Patricia V Pietrantonio,Cecilia Tamborindeguy,Olena Riabinina

doi:10.1371/journal.pone.0216800

Abstract

The reproductive ground plan hypothesis proposes that gene networks regulating foraging behavior and reproductive female physiology in social insects emerged from ancestral gene and endocrine factor networks. Expression of storage proteins such as vitellogenins and hexamerins is an example of this co-option. Hexamerins, through their role modulating juvenile hormone availability, are involved in caste determination in termites. The genome of the fire ant (Solenopsis invicta) encodes four hexamerin genes, hexamerin-like (LOC105192919, hereafter called hexamerin 1), hexamerin (LOC105204474, hereafter called hexamerin 2), arylphorin subunit alpha-like, and arylphorin subunit beta. In this study, a phylogenetic analysis of the S. invicta hexamerins determined that each predicted protein clustered with one of the orthologous Apis mellifera hexamerins. Gene expression analyses by RT-qPCR revealed differential expression of the hexamerins between queens and workers, and between specific task-allocated workers (nurses and foragers). Queens and nurses had significantly higher expression of all genes when compared to foragers. Hexamerin 1 was expressed at higher levels in queens, while hexamerin 2 and arylphorin subunit beta were expressed at significantly higher levels in nurses. Arylphorin subunit alpha-like showed no significant difference in expression between virgin queens and nurses. Additionally, we analyzed the relationship between the expression of hexamerin genes and S-hydroprene, a juvenile hormone analog. Significant changes in hexamerin expression were recorded in nurses, virgin queens, and foragers 12 h after application of the analog. Hexamerin 1 and arylphorin subunit alpha-like expression were significantly lower after analog application in virgin queens. In foragers, hexamerin 2 and arylphorin subunit beta were significantly lower after analog application, while in nurses expression of all genes were significantly lower after analog application. Our results suggest that in S. invicta hexamerin genes could be associated with reproductive division of labor and task-allocation of workers.

Highlights

The reproductive ground plan hypothesis proposes that the gene networks that regulate foraging behavior and reproductive female physiology in social insects emerged from ancestral networks of genes and endocrine factors [1,2,3]
In this study, we evaluated the expression of the four hexamerin genes in S. invicta workers and queens, and investigated whether those genes were regulated by a juvenile hormone (JH) analog in a casteor task-specific manner
Four hexamerin genes are predicted in the S. invicta genome (LOC105192919, LOC105192898, LOC105204474, and LOC105192897)

Summary

Introduction

The reproductive ground plan hypothesis proposes that the gene networks that regulate foraging behavior and reproductive female physiology in social insects emerged from ancestral networks of genes and endocrine factors [1,2,3]. Examples of this co-option of gene networks to regulate division of labor have been shown in several social hymenopteran species [4,5,6,7]. Pogonomyrmex barbatus nurses express high levels of Vg transcript which decrease as the individual transitions into foraging tasks [14]. In Ectatomma tuberculatum, production of Vg is related to the worker age: workers produce high levels of Vg at the beginning of their adult life when they conduct tasks associated with the brood inside the nest, while older workers which perform tasks outside the nest do not produce Vg [15]

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Conclusion