Abstract
The evolution of obligate kleptoparasitism, the theft of food, has led to remarkable innovations, including physical weapons and chemical signals that can evolve into chemical weapons. Stingless bees in the genus Lestrimelitta are excellent examples of this phenomenon because they are obligate kleptoparasites that no longer collect floral resources and instead steal brood resources from other bees. Their ability to raid successfully is thus essential to their fitness even when they fight species that are physically bigger, have larger defense forces, or both. We conducted morphometric analyses, quantified Lestrimelitta niitkib mandibular gland pheromone (MGP) components, and carried out individual fighting trials between L. niitkib and the stingless bee Scaptotrigona mexicana, a common victim species, to shed light on the detailed reasons for their success at robbing. Measurements showed that L. niitkib mandibles have thicker exoskeleton cuticles and overall greater width, particularly in the medial and proximal sections, than S. mexicana, which is quite similar in body size. In all fights, L. niitkib bit victims and released MGP, as it does during raids. Scaptotrigona mexicana victims exhibited significantly increased uncoordinated behaviors and showed partial or complete paralysis. We analyzed and quantified the major components of MGP, which consisted of large quantities of geranial (mean of 253 μg) and neral (48 μg) per bee. Microinjections of 1 bee equivalent (BE) of natural or synthetic MGP and ≥ 0.1 BE of geranial significantly increased deleterious behaviors and paralysis as compared to control injections. We suggest that the large quantities of MGP used during raiding have led to an unexpected outcome, a semiochemical evolving the additional function of a toxin, and contribute to the ability of Lestrimelitta to rob its victims.Significance statementKleptoparasites, organisms that steal food resources, employ multiple physical and chemical tools to survive. The success of kleptoparasitism requires a balance between honesty and coercion in interspecific communication. The genus Lestrimellita consists of a group of kleptoparasitic stingless bee species that raid other bee colonies for food and therefore depend upon winning these raids. However, why they succeed remains not fully understood. We studied differences in morphology between L. niitkib and its victims, the pheromones they release during raids, and ran individual fight trials between L. niitkib and a common victim to identify why they are successful. We suggest that the release of pheromones at the beginning of raids, in concert with the pheromone’s toxicity, has been combined to improve L. niitkib’s ability to successfully rob.
Highlights
The roles of honesty and coercion in the evolution of chemical signals have been extensively debated (Villalta et al 2018; Orlova and Amsalem 2019) and extended to communication between different species (Brown et al 1970; Ruther et al 2002; Garvey et al 2017)
We studied differences in morphology between L. niitkib and its victims, the pheromones they release during raids, and ran individual fight trials between L. niitkib and a common victim to identify why they are successful
L. nittkib had thicker mandibular cuticles (Fig. 1b) and wider average mandible widths than S. mexicana, which is very similar in body size based upon a common allometric measure of bee body size, the intertegular distance (L. nittkib 1.51 ± 0.02 mm, S. mexicana 1.48 ± 0.03 mm)
Summary
The roles of honesty and coercion in the evolution of chemical signals have been extensively debated (Villalta et al 2018; Orlova and Amsalem 2019) and extended to communication between different species (Brown et al 1970; Ruther et al 2002; Garvey et al 2017). If the chemical signal is a toxin (i.e., an allomone, Brown et al 1970) such as formic acid in ant venom glands (Hölldobler et al 1990) or in the mandibular gland secretions of Oxytrigona stingless bees (Roubik et al 1987), signal honesty should theoretically be reinforced. This potential for a signal to become venom-like is poorly understood
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