Pheromones and other kinds of chemical communication underlie the behavior of all animals Building on the strengths of the first edition, widely recognized as the leading text in the subject, this is a comprehensive overview of how pheromones work Extensively revised and expanded to cover advances made over the last ten years, the book offers a thorough exploration of the evolutionary and behavioral contexts of chemical communication along with a detailed introduction to the molecular and neural basis of signal perception through olfaction At a time of ever increasing specialization, Wyatt offers a unique synthesis, integrating examples across the animal kingdom A final chapter critically considers human pheromones and the importance of olfaction to human biology Its breadth of coverage and readability make the book an unrivaled resource for students and researchers in a range of fields from chemistry, genetics, genomics, molecular biology and neuroscience to ecology, evolution and behavior

Pheromones and Animal Behavior: Chemical Signals and Signatures

Pheromones have been found in species in almost every part of the animal kingdom, including mammals. Pheromones (a molecule or defined combination of molecules) are species-wide signals which elicit innate responses (though responses can be conditional on development as well as context, experience, and internal state). In contrast, signature mixtures, in invertebrates and vertebrates, are variable subsets of molecules of an animal’s chemical profile which are learnt by other animals, allowing them to distinguish individuals or colonies. All signature mixtures, and almost all pheromones, whatever the size of molecules, are detected by olfaction (as defined by receptor families and glomerular processing), in mammals by the main olfactory system or vomeronasal system or both. There is convergence on a glomerular organization of olfaction. The processing of all signature mixtures, and most pheromones, is combinatorial across a number of glomeruli, even for some sex pheromones which appear to have ‘labeled lines’. Narrowly specific pheromone receptors are found, but are not a prerequisite for a molecule to be a pheromone. A small minority of pheromones act directly on target tissues (allohormone pheromones) or are detected by non-glomerular chemoreceptors, such as taste. The proposed definitions for pheromone and signature mixture are based on the heuristic value of separating these kinds of chemical information. In contrast to a species-wide pheromone, there is no single signature mixture to find, as signature mixtures are a ‘receiver-side’ phenomenon and it is the differences in signature mixtures which allow animals to distinguish each other.

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Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates.

1 Introduction Henrik Brumm Part I: Signal Detection Theory 2 Signal Detection, Noise, and the Evolution of Communication R. Haven Wiley Part II: Acoustic Signals 3 Masking by Noise in Acoustic Insects: Problems and Solutions Heiner Romer 4 Effects of Noise on Sound Detection and Acoustic Communication in Fishes Friedrich Ladich 5 Anuran Acoustic Signal Production in Noisy Environments Joshua J. Schwartz and Mark A. Bee 6 Anuran Acoustic Signal Perception in Noisy Environments Alejandro Velez, Joshua J. Schwartz, and Mark A. Bee 7 Avian Vocal Production in Noise Henrik Brumm and Sue Anne Zollinger 8 Avian Sound Perception in Noise Robert J. Dooling and Sandra H. Blumenrath 9 Effects of Noise on Acoustic Signal Production in Marine Mammals. Peter L. Tyack and Vincent M. Janik 10 Effects of Noise on Sound Perception in Marine Mammals James J. Finneran and Brian K. Branstetter Part III: Optical, Electric, and Chemical Signals 11 Noise in Visual Communication: Motion from Wind-Blown Plants Richard A Peters 12 Neural Noise in Electro communication -from Burden to Benefits Jan Benda, Jan Grewe and Rudiger Krahe 13 Noise in Chemical Communication Volker Nehring, Tristram D. Wyatt and Patrizia d'Ettorre Part IV: Impacts of Anthropogenic Noise 14. Anthropogenic Noise and Conservation Peter K. McGregor, Andrew G. Horn, Marty L. Leonard and, Frank Thomsen

Animal communication and noise

Murine Pheromone Proteins Constitute a Context-Dependent Combinatorial Code Governing Multiple Social Behaviors

Synchronous evolution of an odor biosynthesis pathway and behavioral response

Among invertebrates, specific pheromones elicit inherent (fixed) behavioural responses to coordinate social behaviours such as sexual recognition and attraction. By contrast, the much more complex social odours of mammals provide a broad range of information about the individual owner and stimulate individual-specific responses that are modulated by learning. How do mammals use such odours to coordinate important social interactions such as sexual attraction while allowing for individual-specific choice? We hypothesized that male mouse urine contains a specific pheromonal component that invokes inherent sexual attraction to the scent and which also stimulates female memory and conditions sexual attraction to the airborne odours of an individual scent owner associated with this pheromone. Using wild-stock house mice to ensure natural responses that generalize across individual genomes, we identify a single atypical male-specific major urinary protein (MUP) of mass 18893Da that invokes a female's inherent sexual attraction to male compared to female urinary scent. Attraction to this protein pheromone, which we named darcin, was as strong as the attraction to intact male urine. Importantly, contact with darcin also stimulated a strong learned attraction to the associated airborne urinary odour of an individual male, such that, subsequently, females were attracted to the airborne scent of that specific individual but not to that of other males. This involatile protein is a mammalian male sex pheromone that stimulates a flexible response to individual-specific odours through associative learning and memory, allowing female sexual attraction to be inherent but selective towards particular males. This 'darcin effect' offers a new system to investigate the neural basis of individual-specific memories in the brain and give new insights into the regulation of behaviour in complex social mammals. See associated Commentary http://www.biomedcentral.com/1741-7007/8/71

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Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour

Many mammals use scent marking for sexual and competitive advertisement, but little is known about the mechanism by which scents are used to locate mates and competitors. We show that darcin, an involatile protein sex pheromone in male mouse urine, can rapidly condition preference for its remembered location among females and competitor males so that animals prefer to spend time in the site even when scent is absent. Learned spatial preference is conditioned through contact with darcin in a single trial and remembered for approximately 14 days. This pheromone-induced learning allows animals to relocate sites of particular social relevance and provides proof that pheromones such as darcin can be highly potent stimuli for social learning.

https://science.sciencemag.org/content/sci/338/6113/1462.full.pdf

Pheromonal Induction of Spatial Learning in Mice

Reliable recognition of individuals requires phenotypic identity signatures that are both individually distinctive and appropriately stable over time. Individual-specific vocalisations or visual patterning are well documented among birds and some mammals, whilst odours play a key role in social recognition across many vertebrates and invertebrates. Less well understood, though, is whether individuals are recognised through variation in cues that arise incidentally from a wide variety of genetic and non-genetic differences between individuals, or whether animals evolve distinctive polymorphic signals to advertise identity reliably. As a bioassay to understand the derivation of individual-specific odour signatures, we use female attraction to the individual odours of male house mice (Mus musculus domesticus), learned on contact with a male’s scent marks. Learned volatile odour signatures are determined predominantly by individual differences in involatile major urinary protein (MUP) signatures, a specialised set of communication proteins that mice secrete in their urine. Recognition of odour signatures in genetically distinct mice depended on differences in individual MUP genotype. Direct manipulation using recombinant MUPs confirmed predictable changes in volatile signature recognition according to the degree of matching between MUP profiles and the learned urine template. Both the relative amount of the male-specific MUP pheromone darcin, which induces odour learning, and other MUP isoforms influenced learned odour signatures. By contrast, odour recognition was not significantly influenced by individual major histocompatibility complex genotype. MUP profiles shape volatile odour signatures through isoform-specific differences in binding and release of urinary volatiles from scent deposits, such that volatile signatures were recognised from the urinary protein fraction alone. Manipulation using recombinant MUPs led to quantitative changes in the release of known MUP ligands from scent deposits, with MUP-specific and volatile-specific effects. Despite assumptions that many genes contribute to odours that can be used to recognise individuals, mice have evolved a polymorphic combinatorial MUP signature that shapes distinctive volatile signatures in their scent. Such specific signals may be more prevalent within complex body odours than previously realised, contributing to the evolution of phenotypic diversity within species. However, differences in selection may also result in species-specific constraints on the ability to recognise individuals through complex body scents.

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Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs)

Female attraction to male scent and associative learning: the house mouse as a mammalian model

When hybridisation carries a cost, natural selection is predicted to favour evolution of traits that allow assortative mating (reinforcement). Incipient speciation between the two European house mouse subspecies, Mus musculus domesticus and M.m.musculus, sharing a hybrid zone, provides an opportunity to understand evolution of assortative mating at a molecular level. Mouse urine odours allow subspecific mate discrimination, with assortative preferences evident in the hybrid zone but not in allopatry. Here we assess the potential of MUPs (major urinary proteins) as candidates for signal divergence by comparing MUP expression in urine samples from the Danish hybrid zone border (contact) and from allopatric populations. Mass spectrometric characterisation identified novel MUPs in both subspecies involving mostly new combinations of amino acid changes previously observed in M.m.domesticus. The subspecies expressed distinct MUP signatures, with most MUPs expressed by only one subspecies. Expression of at least eight MUPs showed significant subspecies divergence both in allopatry and contact zone. Another seven MUPs showed divergence in expression between the subspecies only in the contact zone, consistent with divergence by reinforcement. These proteins are candidates for the semiochemical barrier to hybridisation, providing an opportunity to characterise the nature and evolution of a putative species recognition signal.

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Sarah A. Roberts

Papers

Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour

Pheromonal Induction of Spatial Learning in Mice

Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs)

Female attraction to male scent and associative learning: the house mouse as a mammalian model

Molecular heterogeneity in major urinary proteins of Mus musculus subspecies: potential candidates involved in speciation.