Odor coding of nestmate recognition in the eusocial ant Camponotus floridanus

Abstract

In eusocial ants, aggressive behaviors require the ability to discriminate between chemical signatures such as cuticular hydrocarbons that distinguish nestmate friends from non-nestmate foes. It has been suggested that a mismatch between a chemical signature (label) and the internal, neuronal representation of the colony odor (template) leads to aggression between non-nestmates. Moreover, a definitive demonstration that odorant receptors are responsible for the processing of the chemical signals that regulate nestmate recognition has thus far been lacking. To address these issues, we have developed an aggression-based bioassay incorporating highly selective modulators that target odorant receptor functionality to characterize their role in nestmate recognition in the formicine ant Camponotus floridanus. Electrophysiological studies were used to show that exposure to either a volatilized antagonist or an agonist eliminated or dramatically altered signaling, respectively. Administration of these compounds to adult workers significantly reduced aggression between non-nestmates without altering aggression levels between nestmates. These studies provide direct evidence that odorant receptors are indeed necessary and sufficient for mediating aggression towards non-nestmates. Furthermore, our observations support a hypothesis in which rejection of non-nestmates depends on the precise decoding of chemical signatures present on non-nestmates as opposed to the absence of any information or the active acceptance of familiar signatures.

Genetic Underpinnings of Host Manipulation byOphiocordycepsas Revealed by Comparative Transcriptomics

“…Its homolog in C. castaneus was significantly downregulated (fourfold decrease) (de Bekker et al 2015). However, up-or downregulation of orco may lead to similar phenotypes as both agonist and antagonist effects on Orco are reported to produce similar changes in C. floridanus nestmate recognition (Ferguson et al 2020). Similarly, in both ant host species, multiple genes putatively encoding PBP Gp9 were differentially expressed during manipulation (de Bekker et al 2015) (File S3) and have been implicated in mediating fire ant colony social dynamics (Ross 1997;Ross and Keller 1998;Krieger and Ross 2002;.…”

“…One of the odorant receptors, putatively encoding an odorant receptor coreceptor (Orco), is highly conserved in insects and has a central role in odor detection (Jones et al 2005;Stengl and Funk 2013;Zhou et al 2014;Lin et al 2015). Dysregulation of orco in ants has been linked to changes in overall sensitivity to odorants, and affects behavior such as time spent outside the nest, ability to detect prey, and aggression toward conspecifics (Yan et al 2017;Ferguson et al 2020). One of two putative orco genes in C. floridanus was significantly upregulated in the ant during live manipulation compared to control (threefold increase).…”

Expansion and Accelerated Evolution of 9-Exon Odorant Receptors inPolistesPaper Wasps

“…This is characteristic of combinatorial coding: the process of combining input from multiple ORs that bind overlapping sets of ligands in order to discriminate a larger variety of odors ( Malnic et al 1999 ; Touhara and Vosshall 2009 ). Functional ORs are necessary for normal nesting behavior and for nestmate recognition in ants, a process which involves detecting variation in the CHCs on the cuticles of conspecifics ( Lavine et al 1990 ; van Zweden and d’ Ettorre 2010 ; Sturgis and Gordon 2012 ; Trible et al 2017 ; Yan et al 2017 ; Ferguson et al 2020 ). Together these studies suggest that 9-exon ORs function in combinatorial coding of CHC perception in ants and potentially in general across Hymenoptera.…”

Advances in the Study of Olfaction in Eusocial Ants

“…To address this confounding factor, we recently took advantage of a set of recently identified, novel pharmacological agents that acutely and selectively modulate Orco activity to examine the role of OR signaling in nestmate recognition [ 128 ]. These compounds include an allosteric agonist, an allosteric antagonist, and a physiologically and pharmacologically inert analog control, all of which can be applied as volatiles to wild-type adult ants.…”