Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: indicators for division of labor and nutritional status?

Paula Castillo,Patricia V Pietrantonio,Deborah M. Gordon

doi:10.1371/journal.pone.0083966

Abstract

In the red imported fire ant, Solenopsis invicta Buren, the neuronal and molecular mechanisms related to worker division of labor are poorly understood. Workers from different subcastes (major, medium and minors) perform different tasks, which are loosely associated with their size. We hypothesized that the short neuropeptide F (sNPF) signaling system (NPY-like) could be involved in mechanisms of worker division of labor and sensing or responding to colony nutritional requirements. Thus, we investigated the expression of the short neuropeptide F receptor (sNPFR) in the brain and subesophageal ganglion (SEG) of workers from colonies with and without brood. Across worker subcastes a total of 9 clusters of immunoreactive sNPFR cells were localized in the brain and the subesophageal ganglion (SEG); some of these cells were similar to those observed previously in the queen. Worker brain sNPFR cell clusters were found in the protocerebrum near mushroom bodies, in the central complex and in the lateral horn. Other sNPFR immunoreactive cells were found at the edge of the antennal lobes. Across subcastes, we observed both a constant and a differential pattern of sNPFR clusters, with a higher number of sNPFR cells found in minor than in major workers. Those sNPFR cells detected in all worker subcastes appear to be involved in olfaction or SEG functions. The differential expression of clusters in subcastes suggests that sNPFR signaling is involved in regulating behaviors associated with specific subcastes and thus, division of labor. Some sNPFR cells appear to be involved in nutrient sensing and/or brood care, feeding behavior and locomotion. In colonies without brood, workers showed a lower cluster number, and an overall reduced sNPFR signal. Our results suggest the sNPF signaling system is a candidate for the neurobiological control of worker division of labor and sensing brood presence, perhaps correlating with protein requirements and availability.

Highlights

The red imported fire ants (Solenopsis invicta Buren; Hymenoptera: Formicidae) are eusocial insects native from South America with an extraordinary capacity for adaptation to different environments
We focused on the immunolocalization of the short neuropeptide F receptor in the brain of fire ant workers, investigating if there is a relationship between the sNPF/sNPFR signaling pathway and worker division of labor, and their sensing/or responding to colony nutritional requirements, which could be affected by the presence or absence of brood
Based on the dynamic changes found in the sNPF peptide in honey bee worker brains in response to nutritional cues and foraging behavior, we investigated the distribution of the sNPFR in the brain of fire ants workers in colonies with and without brood

Summary

Introduction

The red imported fire ants (Solenopsis invicta Buren; Hymenoptera: Formicidae) are eusocial insects native from South America with an extraordinary capacity for adaptation to different environments They have invaded countries such as the United States, Australia, New Zealand, China and Taiwan [1]. Fire ant colonies are composed by individuals from different castes, designated as the reproductives (males and females) and the workers This reproductive division of labor refers to specialization of drones and queens for the generation of new individuals, while female worker ants co-operate and perform brood rearing, care for the queen, forage for food, defend the nest, dig soil for nest construction, etc. In other ants and bees the endocrine mechanism appears to be related to a higher juvenile hormone titer in older workers that promotes foraging in comparison to younger nurses that remain in the nest [7]

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