Research report
The evolution of pheromonal communication

https://doi.org/10.1016/j.bbr.2008.09.039Get rights and content

Abstract

Small-brained rodents have been the principle focus for pheromonal research and have provided comprehensive insights into the chemosensory mechanisms that underpin pheromonal communication and the hugely important roles that pheromones play in behavioural regulation. However, pheromonal communication does not start or end with the mouse and the rat, and work in amphibians reveals much about the likely evolutionary origins of the chemosensory systems that mediate pheromonal effects. The dual olfactory organs (the main olfactory epithelium and the vomeronasal organ), their receptors and their separate projection pathways appear to have ancient evolutionary origins, appearing in the aquatic ancestors of all tetrapods during the Devonian period and so pre-dating the transition to land. While the vomeronasal organ has long been considered an exclusively pheromonal organ, accumulating evidence indicates that it is not the sole channel for the transduction of pheromonal information and that both olfactory systems have been co-opted for the detection of different pheromone signals over the course of evolution. This has also led to great diversity in the vomeronasal and olfactory receptor families, with enormous levels of gene diversity and inactivation of genes in different species. Finally, the evolution of trichromacy as well as huge increases in social complexity have minimised the role of pheromones in the lives of primates, leading to the total inactivation of the vomeronasal system in catarrhine primates while the brain increased in size and behaviour became emancipated from hormonal regulation.

Introduction

Fifty years ago, Karlson and Luscher [43] coined the term ‘pheromone’ to describe chemicals released by animals into the environment which have consistent effects on the behaviour or physiology of conspecifics, akin to the effects of hormones on the internal physiology of the individual. In so doing they recognised that pheromones are distinct from other semiochemicals which communicate biological information whether intended or not and whether to a conspecific or heterospecific. Since then, research across different disciplines has enormously advanced our understanding of the chemistry of pheromones, the sensory systems which detect them and the neurochemical pathways which transduce these signals. The importance of pheromonal communication has evolved over time and varies considerably between species, and this has significant effects on pheromonal signals and the sensory systems that detect them. Major evolutionary changes such as the transition from water to land have had a huge effect on pheromonal communication in tetrapods, changing the key chemical property of pheromones from solubility to volatility, modifying the mechanisms of pheromone release into these mediums, and resulting in major changes in morphology and function of sensory organs, as well as in the receptors that bind pheromone ligands [24]. However, other less obvious evolutionary changes have also had considerable consequences for the importance of pheromones in behaviour, particularly in mammals. This review is intended to provide an overview of how pheromonal communication in tetrapods has changed and of the factors that are thought to have driven these adaptations. The majority of research into pheromonal communication in vertebrates has focused on mammals, and particularly on rodents. It is this work that has illuminated the fundamental processes involved in the detection of pheromonal signals by chemosensory organs, the molecular biology of signal transduction in these sensory systems, and the forebrain pathways that are involved in triggering behavioural responses to pheromones. However, to understand the evolutionary roots of the systems at work in mammals, we must consider pheromonal communication in other animal classes, such as amphibians, which can tell us much about the evolution of the dual olfactory systems and their origins in the ancestors of tetrapods [23]. While pheromonal communication is a key regulatory component of behaviour in small-brained mammals, it has diminished in importance in larger-brained primates, where the evolution of trichromacy and the expansion of the cortex have combined to reduce the role of pheromones in modulating endocrine responses and regulating behaviour [15]. The evolutionary pressures of new ecological niches and increased social complexity drove the expansion of the cortex in primates and a consequent decline in the importance of pheromonal regulation of behaviour.

Section snippets

Pheromonal signals

Pheromones are major modulators of behaviour in most mammals, regulating behaviours including reproduction, maternal care, aggression and alarm responses (see Table 1). Pheromones have traditionally been defined as either ‘releasers’ which trigger immediate short-term behavioural responses, or ‘primers’ which trigger medium to long-term changes in behaviour or physiology. A third class of pheromones, ‘signallers’, has been added to these classical categories to describe chemosignals which carry

Amphibian pheromones

While the majority of research into MOE and VNO function has been conducted in mammals, these dual olfactory systems appear to have evolved in ancestral tetrapods, meaning that a great deal can be learnt about these evolutionary origins by studying pheromonal communication in amphibians. There are three main extant groups of amphibians, the anurans (toads and frogs), the caudates/urodeles (newts and salamanders) and the caecilians. The salamanders and frogs have been the main subjects for

Dual olfactory systems in mammals

The evolving importance of pheromonal communication in mammals has driven major changes in chemosensation, which are reflected in the functions of the dual olfactory systems and in the diversity of the gene families that encode MOE and VNO receptors in different species. While most mammals have both olfactory systems, the vomeronasal system is not present in marine mammals [65], bats [85], old world monkeys and great apes (catarrhine primates) [49]. While the aquatic and arboreal environments

Human pheromones

The possible regulation of human behaviour by pheromones is a topic that arouses interest and controversy in equal measure in the scientific community as well as the wider public. Several studies have demonstrated physiological and psychological responses to semiochemicals in humans, however it is clear that these are very different to the effects that pheromones exert on behaviour in small-brained mammals. The odours of females in the ovulatory phase of the menstrual cycle have been shown to

Conclusion

Pheromonal communication in tetrapods has evolved to regulate diverse behaviours in very different species, employing varied signals to communicate both very complex and very simple messages. While certain behavioural responses in some species are robust and consistent, others are shaped by the identities of the signaller and receiver and the relationships between them. These signals are detected primarily by the VNO in mammals, however the MOE also plays a significant role in the detection of

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