Abstract

In several highly eusocial insect species with morphologically distinct castes, queen-characteristic cuticular hydrocarbons (CHCs) have been shown to act as queen signals that suppress the reproduction of nestmate workers. However, it is not known whether such queen pheromones might also play a role in regulating reproductive division of labour in primitively eusocial insects that lack morphologically defined castes. Here, we experimentally tested whether a blend of CHCs which occurred in higher concentrations in the dominant breeding female act as a queen pheromone, and inhibit reproduction by subordinate females in the primitively eusocial paper wasp Polistes satan. In contrast to earlier findings with highly eusocial species, our results show that although specific compounds were enhanced in dominant, reproductively active females, a blend of five of these compounds did not inhibit development of the ovaries of female nestmates. Instead, the dominant female had to be physically present to prevent subordinate females from reproducing. Our results are in line with earlier evidence suggesting that fertility-linked compounds in primitively eusocial wasps act only as cues and help to regulate reproduction when used in conjunction with aggressive dominance behaviour, meaning the physical presence of the dominant female. Alternatively, our results support the hypothesis that queen pheromones in highly eusocial insects were co-opted from fertility cues that were already present in primitively eusocial ancestors, even when initially, such compounds were merely produced as by-products of ovarian activation, without actually serving to signal reproductive status.

Highlights

  • The reproductive division of labor between fertile queens and sterile workers in highly eusocial insects has been found to be regulated by queen pheromones (Peeters and Liebig, 2009; Holman, 2010; van Zweden, 2010; Kocher and Grozinger, 2011; Richard and Hunt, 2013; Oi et al, 2015; Grüter and Keller, 2016)

  • The idea that hydrocarbons may act as queen or fertility signals originally was supported by purely correlative evidence, including observations that fertile and non-fertile colony members consistently differed in their cuticular hydrocarbons (CHCs) profiles (Monnin, 2006; Peeters and Liebig, 2009; Liebig, 2010), that CHC profiles correlated with variation in fecundity within a given caste (d’Ettorre et al, 2004; Heinze, 2004; Endler et al, 2006; Holman et al, 2010a,b; van Zweden et al, 2014), and that workers discriminated between the CHC profiles of fertile and nonfertile individuals (Dietemann et al, 2003; Heinze, 2004)

  • There was no evidence that the presence of higher numbers of inseminated females affected the mean probability of subordinate females to activate their ovaries (binomial Generalized Linear Mixed-effect Model (GLMM) with number of mated females coded as an z-value p-value (A) (Intercept) Blend Queenright Colony size (B) (Intercept) Blend Spermatheca additional covariate, z = −1.42, p = 0.16, Table S4)

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Summary

Introduction

The reproductive division of labor between fertile queens and sterile workers in highly eusocial insects has been found to be regulated by queen pheromones (Peeters and Liebig, 2009; Holman, 2010; van Zweden, 2010; Kocher and Grozinger, 2011; Richard and Hunt, 2013; Oi et al, 2015; Grüter and Keller, 2016). These pheromones signal the presence of a healthy and fertile queen, to which the workers generally. One might expect that in these species, queen pheromones that signaled the queen’s high fecundity would be intrinsically evolutionarily stable, and that the queen would not have to physically aggress workers to be able to maintain her reproductive dominance

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