Pheromonal control: reconciling physiological mechanism with signalling theory

Abstract

Pheromones are intraspecific chemical signals. They can have profound effects on the behaviour and/or physiology of the receiver, and it is still common to hear pheromones described as controlling of the behaviour of the receiver. The discussion of pheromonal control arose initially from a close association between hormones and pheromones in the comparative physiological literature, but the concept of a controlling pheromone is at odds with contemporary signal evolution theory, which predicts that a manipulative pheromonal signal negatively affecting the receiver's fitness should not be stable over evolutionary time. Here we discuss the meaning of pheromonal control, and the ecological circumstances by which it might be supported. We argue that in discussing pheromonal control it is important to differentiate between control applied to the effects of a pheromone on a receiver's physiology (proximate control), and control applied to the effects of a pheromone on a receiver's fitness (ultimate control). Critically, a pheromone signal affecting change in the receiver's behaviour or physiology need not necessarily manipulate the fitness of a receiver. In cases where pheromonal signalling does lead to a reduction in the fitness of the receiver, the signalling system would be stable if the pheromone were an honest signal of a social environment that disadvantages the receiver, and the physiological and behavioural changes observed in the receiver were an adaptive response to the new social circumstances communicated by the pheromone.

Diet-Mediated Pheromones and Signature Mixtures Can Enforce Signal Reliability

“…Nonetheless, comprehensive studies that include both behavioral and chemical assays are largely limited to insect systems. For example, studies on mammals are typically behavioral, and although this is consistent with other pheromone research, future studies should consider combining behavioral assays with chemical analyses in these groups (Peso et al, 2015).…”

“…Pheromones alter the behavior of another organism and evolve precisely because of the nature of this effect (Maynard Smith and Harper, 2003). The receiver's capacity to detect and respond to the signal has similarly evolved to maximize detection (see Peso et al, 2015), thereby optimizing the effectiveness of pheromones. Wyatt (2010) distinguishes between pheromones, which typically elicit a predisposed response in the receiver, and signature mixtures that first require the receiver to learn the chemical signal.…”

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

“…In highly eusocial insect species with large colonies, chemical signals are often used. These signals allow an efficient reproductive division of labour across a large social group, reduce the use of costly behaviours that hamper the group's productivity, and provide a more efficient and precise way to regulate multiple complex behaviours [1][2][3].…”

Solitary bees reduce investment in communication compared with their social relatives

“…Some of these pheromones contain compounds that can be highly conserved across species, suggesting that there may be some aspects of these blends that have been coopted from the mating or defense signals of their solitary ancestors (16). Although several comparative studies have examined the evolution of these compounds across social insect species (17)(18)(19)(20), the focus has been primarily on their role as either reliable indicators of reproductive status or a mechanism of queen manipulation to render workers sterile (21,22).…”