Cuticular hydrocarbons correlate with queen reproductive status in native and invasive Argentine ants (Linepithema humile, Mayr)

Sílvia Abril,Alain Lenoir,Carolina Ivon Paris,Mireia Diaz,Raphaël Boulay,Crisanto Gómez,Fabio S Nascimento

doi:10.1371/journal.pone.0193115

Abstract

In insect societies, chemical communication plays an important role in colony reproduction and individual social status. Many studies have indicated that cuticular hydrocarbons (CHCs) are the main chemical compounds encoding reproductive status. However, these studies have largely focused on queenless or monogynous species whose workers are capable of egg laying and have mainly explored the mechanisms underlying queen-worker or worker-worker reproductive conflicts. Less is known about what occurs in highly polygynous ant species with permanently sterile workers. Here, we used the Argentine ant as a model to examine the role of CHCs in communicating reproductive information in such insect societies. The Argentine ant is unicolonial, highly polygynous, and polydomous. We identified several CHCs whose presence and levels were correlated with queen age, reproductive status, and fertility. Our results also provide new insights into queen executions in the Argentine ant, a distinctive feature displayed by this species in its introduced range. Each spring, just before new sexuals appear, workers eliminate up to 90% of the mated queens in their colonies. We discovered that queens that survived execution had different CHC profiles from queens present before and during execution. More specifically, levels of some CHCs were higher in the survivors, suggesting that workers could eliminate queens based on their chemical profiles. In addition, queen CHC profiles differed based on season and species range (native vs. introduced). Overall, the results of this study provide new evidence that CHCs serve as queen signals and do more than just regulate worker reproduction.

Highlights

Social insects are good models for studying chemical communication since their striking selforganisation and division of labour involve sophisticated chemical systems
De Biseau and colleagues [42] had already demonstrated that ovarian activity is correlated with the cuticular hydrocarbons (CHCs) profiles in queens of this ant species, their results were mainly qualitative. We explore this point more in depth by: 1) adding a new reproductive variable, the egg-laying rate, something nonexplored before in this ant species in relation to the CHC profiles of queens, and 2) searching for certain CHCs correlated with fertility that could signal reproductive information
The CHC profiles of Argentine ant queens displayed a complex mixture of linear, methylbranched, di methyl-branched, and tri-methyl-branched alkanes, as well as some alkenes and one alkadiene; these CHCs ranged from C25 to C36, a wider range than reported in previous studies [41, 42]

Summary

Introduction

Social insects are good models for studying chemical communication since their striking selforganisation and division of labour involve sophisticated chemical systems. According to Keller and Nonacs [1], queens produce honest fertility signals to which workers react by refraining from reproducing or preventing other workers from doing so (i.e., worker policing, sensu Ratnieks [2]) This system allows queens to maintain reproductive supremacy within the colony, while allowing workers to accurately assess queen health and fertility and react as needed to increase colony reproductive efficiency and, their own inclusive fitness [1, 3, 4]. Many studies have indicated that cuticular hydrocarbons (CHCs) are the main queen signals—they encode information about queen reproductive status and fertility (see [3,4,5,6,7]) These studies have largely focused on queenless or monogynous species whose workers are capable of egg laying and have mainly explored the mechanisms underlying queenworker or worker-worker conflicts. How can workers manage the colony’s reproductive output when they have dozens of queens to care for? More interestingly, how is the situation handled in large polydomous colonies, which comprise thousands of individuals? Under these circumstances, information sharing between queens and workers should be highly efficient and involve chemically complex queen signals that allow workers to regulate queen fertility and increase colony reproduction [1]

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Conclusion