A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees ( Bombus impatiens )

Abstract

The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees (Bombus terrestris), pentacosane ( C 25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee (Bombus impatiens) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons ( C 23, C 25 and C 27) on the cuticular surfaces of females and tested their effects on the two worker types. Our results indicate differences in responses of naive and experienced workers, genetic effects on worker reproduction, and general effects of hydrocarbons and duration of egg laying on ovary resorption rates. However, we found no evidence to support the theory that a conserved class of hydrocarbons serve as queen pheromones or queen signals in Bombus impatiens.

Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens

“…However, exposure of queenless Bombus impatiens worker groups to pentacosane did not significantly impact ovary activation rates or terminal oocyte sizes after 10 days of exposure [23]. Furthermore, in this study [23], ‘oocyte resorption’ rates were positively correlated with the duration of egg-laying, suggesting this is not an appropriate parameter to quantify reproductive inhibition. Thus, current evidence suggests that queen-produced chemicals alone may only slightly reduce or delay worker reproduction in bumblebees overall.…”

“…The mean of these oocytes for each bee was used as an index of ovary activation [8,13,23]. Newly laid eggs were counted immediately after workers were collected in queenless/caged queen groups, but not in queenright/‘free’ queen worker groups, because it would be impossible to differentiate worker-laid eggs from queen-laid eggs in these groups.…”

“…Comparisons of our behavioural analyses of these two species also support this hypothesis, though without a common garden experiment it is difficult to know if variation in behaviours are due to species-specific differences or differences in environment or observers (see electronic supplementary material, figure S1). Additionally, while ovary activation rates in small queenless worker groups appear to be similar in both species [23,26,27], rates in full-sized late-stage colonies are higher in B. terrestris (50–64%, see [27,28]) than in B. impatiens (9–11%, see [23,29]). Overall, these studies suggest that B. impatiens may rely more heavily on chemical communication to regulate the reproductive division of labour, making comparative studies between B. impatiens and B. terrestris an especially interesting system in which to investigate the transition from aggression to pheromone signalling.…”

Conserved queen pheromones in bumblebees: a reply to Amsalem et al.

“…One exception appears in Table S7 of Amsalem, Orlova & Grozinger (2015), in which the authors fit ANOVAs with CHC treatment, colony, and their interaction as fixed effects. Because of the imbalanced experimental design, the authors chose to discard all the data from colonies a-d (i.e., 46% of the dataset; Table 1) in order to fit the treatment × colony interaction.…”

Preface: Pheromone-Mediation of Female Reproduction and Reproductive Dominance in Social Species

“…However, the ubiquitous occurrence of hydrocarbons, coupled with their easy detection and synthesis through common methodologies, may bias our conclusion regarding their importance in regulating reproductive decisions, compared to the more elaborate chemical signals. Such a bias may further lead to conclusions such as hydrocarbons may act to coercively inhibit worker reproduction or that their role in regulating reproduction in social insects is conserved across taxa (Oi et al 2016; Van Oystaeyen 2014; but see Amsalem et al 2015;Kather and Martin 2015;Nunes et al 2017 for different conclusions). It is not inconceivable that, similar to the highly chemically-diverse alarm or trail pheromones of social insects, pheromone-regulating reproduction are diverse rather than conserved.…”