Regulation of Reproduction in the Primitively Eusocial Wasp Ropalidia marginata: on the Trail of the Queen Pheromone

Abstract

Queens and workers are not morphologically differentiated in the primitively eusocial wasp, Ropalidia marginata. Upon removal of the queen, one of the workers becomes extremely aggressive, but immediately drops her aggression if the queen is returned. If the queen is not returned, this hyper-aggressive individual, the potential queen (PQ), will develop her ovaries, lose her hyper-aggression, and become the next colony queen. Because of the non-aggressive nature of the queen, and because the PQ loses her aggression by the time she starts laying eggs, we hypothesized that regulation of worker reproduction in R. marginata is mediated by pheromones rather than by physical aggression. Based on the immediate loss of aggression by the PQ upon return of the queen, we developed a bioassay to test whether the queen's Dufour's gland is, at least, one of the sources of the queen pheromone. Macerates of the queen's Dufour's gland, but not that of the worker's Dufour's gland, mimic the queen in making the PQ decrease her aggression. We also correctly distinguished queens and workers of R. marginata nests by a discriminant function analysis based on the chemical composition of their respective Dufour's glands.

Identification of an ant queen pheromone regulating worker sterility

“…Moreover, in Camponotus floridanus ants, workers in queenless colonies do not reproduce while queen-laid eggs are present (Endler et al 2004); the eggs are coated with a hydrocarbon mixture similar to the cuticle of queens, consistent with regulation of worker sterility by one or more hydrocarbons. Similarly, queen corpses reduce the reproductive output of live queens in Solenopsis invicta ants (Vargo 1992), and in the wasps Polistes gallicus and Ropalidia marginata queens apparently prevent subordinate reproduction with chemicals from an abdominal gland (Dapporto et al 2007) and Dufour's gland (Bhadra et al 2010), respectively. Interestingly, R. marginata queens had more 3-MeC 31 in Dufour's gland than did workers, suggesting that this compound may act as a primer pheromone in distantly related species.…”

“…Vargo 1992; Peeters et al 1999;Dietemann et al 2003;Cuvillier-Hot et al 2004a;Endler et al 2004;Monnin 2006;Dengler-Crish & Catania 2007;Korb et al 2009;Bhadra et al 2010). However, the honeybee is the only insect in which primer pheromones (i.e.…”

Queen signal should be honest to be involved in maintenance of eusociality: chemical correlates of fertility in Ropalidia marginata

“…Identification of compounds had been done earlier by mass spectrometric analyses (Bhadra et al, 2010). We matched the retention times and pattern of peaks with those obtained in earlier analyses; for statistical analyses, we considered only those peaks that had been identified earlier.…”

“…The Dufour's gland in R. marginata has been shown to be at least one source of the queen pheromone by which queens appear to maintain reproductive monopoly (Bhadra et al, 2010;, presumably by applying the Dufour's gland contents on the nest surface (Bhadra et al, 2007). The Dufour's gland hydrocarbon composition has also been shown to be correlated with ovarian activation status in queens .…”

Stable eusociality via maternal manipulation when resistance is costless

“…In many species, a eusocial colony is composed of one queen and largely non-reproductive workers that are the queen's offspring (Wilson, 1971, Michener, 1974. Whether a queen's offspring becomes a worker or a future queen is often mediated by the queen herself: for example, (1) the queen in some social wasps and bees maintains the reproductive monopoly of the colony through aggression (Fletcher and Ross, 1985); (2) in many social insects the queen can feed offspring with food of different quantity or quality influencing offspring's future reproductive caste (i.e., queen or worker) (e.g., O'Donnell, 1998, Bourke and Ratnieks, 1999, Kapheim et al, 2011, Brand and Chapuisat, 2012; (3) in an ant species the queen can deposit hormones in the eggs inducing offspring to develop into workers (Schwander et al, 2008); (4) in certain wasp and termite species the queen can produce pheromones that prevent offspring from becoming queens (Bhadra et al, 2010, Matsuura et al, 2010; and (5) in honeybees queen pheromones can induce workers to feed larvae without royal jelly causing larvae to develop into workers (Le Conte andHefetz, 2008, Kamakura, 2011). In addition to influencing caste determination, queens can use pheromones to keep workers' ovaries undeveloped (e.g., Holman et al, 2010, Van Oystaeyen et al, 2014, and to alter workers' brain functioning inducing workers to perform various tasks (Beggs et al, 2007).…”