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Pheromones and Other Chemical Communication in Animals☆
Pheromones and Other Chemical Communication in Animalsq Tristram D Wyatt, University of Oxford, Oxford, United Kingdom © 2017 Elsevier Inc. All rights reserved.
Introduction Evolution of Chemical Communication Mechanism of Olfaction, Receptor Proteins, and the Evolution of Pheromones Releaser and Primer Effects of Pheromones Odor Signatures Contrasted With Chemical Signals (Pheromones) Production of Pheromones Range of Roles for Chemical Communication Sex Pheromones Territorial Pheromones Alarm Pheromones Aggregation Pheromones Eavesdropping and Propaganda Techniques for Studying Chemical Communication Exploiting Chemical Communication for Agriculture and Medicine Do Humans Have Pheromones? Conclusions Further Reading Relevant Website
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Introduction Chemical communication is arguably the most widely shared sensory modality, used almost universally across the animal kingdom. From the simplest bacteria to humans, almost all organisms use chemical communication. Within a species, the molecules used for chemical signals are called pheromones. The word pheromone comes from the Greek pherein, to carry or transfer, and horman, to excite or stimulate. Pheromones are often divided by function, such as sex pheromones and aggregation pheromones. A broader term for chemicals involved in animal communication is semiochemical (from the Greek semeion, sign) (Fig. 1). Chemical signals broadcast to the world can also be detected by individuals from other species. So, for example, pheromones
Semiochemicals
Between members of different species
Between members of same species
Signature mixtures
Pheromones
Allelochemicals
species-wide signals
learned by receiver from highly variable chemical profile of conspecific
Allomones
Kairomones
Synomones
benefit emitter, of a different species
benefit receiver, of a different species
benefit both emitter & receiver, of different species
Figure 1 Pheromones are chemical signals used between members of the same species. Pheromones are the same in all sexually mature males, for example, of a species. Individual recognition relies instead on the learning of signature mixtures for individuals (for recognition of siblings for example), based on differences in chemical profile between individuals. Allelochemical is the term given to chemical information received by members of different species. Figure from Wyatt (2014), reprinted with permission from Cambridge University Press.
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Pheromones and Other Chemical Communication in Animals
released by bark beetles may attract their predators – which use the pheromones as a kairomone to locate their bark beetle prey. Chemical signals in deceit or propaganda are termed allomones (discussed in the section titled ‘Eavesdropping and propaganda’). The pheromones above are defined molecules or ratios of particular molecules. All males, for example, of a species produce the same molecules as pheromones, though dominant males may produce more than subordinates, as for example in mice.
Evolution of Chemical Communication Pheromones evolve from chemicals released to the environment that give an advantage to the receiver and the sender. The clue to such an evolutionary path is often given by the identity of the compounds used as pheromones. For example, the sex pheromones released by female goldfish appear to be very similar to the steroid hormones that are circulating in her blood while her eggs are developing. Male goldfish have evolved great sensitivity to these hormone-like compounds. Presumably, over evolutionary time, males able to detect these compounds, initially inadvertently leaking from females, would gain more fertilizations as they would be better able to find the females about to spawn. There would be selection for greater and greater sensitivity in the ‘noses’ of the males – to the extent that now male goldfish can detect the waterborne sex pheromones down to nanomolar and picomolar threshold concentrations. Females would gain more reliable fertilization, so there would be selection for females that, instead of simply leaking these compounds, actually secreted them. Thus, theoretically, something which started as eavesdropping by males could evolve into a pheromone signal produced by females specifically to attract males. Another example comes from the alarm pheromones in ants, released when threatened by a predator or invading ants from another colony. A bizarre variety of compounds are found as alarm pheromones in different taxonomic groups of ants. The pattern is largely explained when the alarm pheromones are compared with the toxic compounds that are released in fighting or defense in those species – the alarm pheromones appear, in many species, to have evolved from defense compounds. Thus all kinds of molecules can potentially evolve to become used as pheromones in chemical communication. The size and stability of compounds can often be related to their role in communication. For example, ant alarm pheromones tend to be small, volatile molecules which diffuse quickly. Hyena territorial marking pheromones are high-molecular- weight involatile compounds, which will last a long time. A wide variety of the compounds are used by different species as pheromones, including steroids, fatty acids, and esters. Some aquatic invertebrates and vertebrates, including amphibians, use short peptides as pheromones. For example, the Asian red-bellied newt (Cynops pyrrhogaster) uses a decapeptide, sodefrin, as its male sex pheromone. The sea slug mollusk Aplysia uses a combination of proteins as its sex pheromone. Small molecules as well as large ones are used by animals large and small. The mammary pheromone of the rabbit, 2-methylbut2-enal, stimulates suckling in rabbit pups. In mammals, some low-molecular-weight pheromones are delivered loosely in the cleft of a protein, which increases the longevity of the signal. For example, small molecule pheromones in the house mouse, such as dehydro-exo-brevicomin, are presented in association with lipocalin major urinary proteins (MUPs), increasing the life of the signal as the small molecules are slowly released. Large quantities of MUPs are present in the urine of dominant male mice. The MUPs may also give some individuality to the signal of the male. One of the MUPs, MUP20 (also known as darcin), is produced by all males and is a male pheromone. When a female mouse sniffs darcin into her vomeronasal organ (VNO) she remembers the location of the male’s scent mark and his individual small molecule odor profile. Some molecules are used as pheromones by unrelated species. For example, brevicomin is used as a pheromone by some bark beetles and dehydro-exo-brevicomin is used by male mice. Such a shared use is not unusual. The Asian elephant (Elephas maximus) shares its female sex pheromone with some 140 species of moth. The compound is a small, volatile molecule, (Z)-7-dodecen-1-yl acetate. This phenomenon comes about because of the common origin of life: basic enzyme pathways are common to all multicellular organisms. In addition, the number of potential different small, and thus volatile, molecules is limited by the number of permutations of combining a small number of atoms. However, moths and elephants are unlikely to be confused by each other as female elephants produce prodigious amounts of the pheromone (and the amounts produced by a female moth will not be noticed by a male elephant) and male moths are attracted to species-specific combinations of pheromone components, of which the elephant pheromone is just one. Most chemical communication, such as that of moths, is by mixtures of small molecules which give species specificity to messages. Female moths’ pheromones tend to consist of a species-specific combination of fatty acids or alcohols. Males respond to the whole blend as a signal. Unique compounds such as the complex molecule supellapyrone, used as a sex pheromone by the brown-banded cockroach, Supella longipalpa, are unusual. However, animals using peptides as their pheromones can have species-specific sequences: another Japanese newt species, Cynops ensicauda uses a decapeptide which differs by two amino acids from the male sex pheromone, sodefrin, of its sister species C. pyrrhogaster. In moths we can see speciation reflected in their chemical communication. Related species may have similar pheromone blends, distinguished by different proportions of the compounds or the addition or loss of certain components. In some moth families, the synthetic pathways for the pheromone blend components are well understood. With this background, the variation in blends produced by different species can be explained by gene frequency changes and mutations, resulting in up- or downregulation of particular enzymes or changes in reaction product or substrate. There may be regional variation in pheromone blends within a moth species, and incipient speciation can sometimes be observed.
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Mechanism of Olfaction, Receptor Proteins, and the Evolution of Pheromones In animals with an olfactory system, with few exceptions pheromones are detected by the olfactory system rather than the gustatory system. The organization of the olfactory system in invertebrates and vertebrates is remarkably similar in functional terms. The great flexibility of the olfactory system means that almost any kind of chemical can potentially evolve into a pheromone if it provides useful information to the receiver. This is because olfaction works by stimulation of a wide range of relatively nonspecific receptor proteins (each expressed on different olfactory sensory neurons linked to glomeruli). The system can respond to the widest possible range of odors, even as entirely new compounds are created (in evolving biological systems). Although a given odor may be unlikely to fit any one receptor perfectly, it is likely to stimulate some. If detection of a molecule gives significant selective advantage, then over evolutionary time, the receptors may evolve great specificity to such molecules; so, for example, on the male moth antennae there are large banks of thousands of olfactory sensory neurons, each with a receptor type very finely tuned to one of the key components of that species’ female sex pheromone. Many vertebrates have a second olfactory system, the vomeronasal organ (VNO), which projects to the accessory olfactory lobe, as well as the main olfactory system. Depending on species, pheromones are detected by either the main olfactory system or the vomeronasal organ or, as seems increasingly likely, both systems. Projections from both systems converge on the amygdala, enabling extensive integration of their chemosensory inputs. Outputs from the medial amygdala lead to pheromone primer effects by activating particular neurons in the hypothalamus.
Releaser and Primer Effects of Pheromones The first pheromones recognized were sex pheromones which elicited (or ‘released’) an almost instantaneous behavioral response. For example, in moths, female sex pheromones elicit orientation flights by males toward the female, and when he finds her, in many species, the male fans his wings as part of courtship. This formed the bioassay used to identify the pheromone (see the section titled ‘Techniques for studying chemical communication’). Some pheromones produce longer-term physiological changes (primer effects) in the receiver. For example, the female goldfish sex pheromones, besides attracting males, also cause the receiving males to increase their sperm and semen production. Primer effects act via the receiver’s endocrine system. There are many interactions between pheromones and the central and the peripheral nervous systems and endocrine systems. Some primer effects can be rapid, and the effects of some behavioral interactions mediated by pheromones can be long lasting. In social insects, queen pheromones with primer effects have been chemically identified in recent years, first in ants then in wasps and bees. These pheromones, independently evolved in each lineage, are produced by the queen in a social insect colony and signal to workers that she is fertile and laying eggs. The reproductive system of the workers is shut down in the presence of queen pheromone. A further class of pheromones, allohormone pheromones, bypass the usual olfactory system of the recipient. A honeybee egg can develop into a worker or a queen. What determines its development is what the larva is fed. If it is fed exclusively with royal jelly, then the genes appropriate for development into a queen are activated. The allohormone pheromone in the royal jelly may include a protein called royalactin which acts on cells in the fat body of the developing larva.
Odor Signatures Contrasted With Chemical Signals (Pheromones) Rather different from pheromones are ‘odor signatures’ which differ between individuals or family groups (or, in social insects, colonies) of the same species. This variability in odor signature makes recognition of individuals or families possible by smell. The odor signature is very complex and is made up from all sources of variation, both genetic and environmental, including recent feeding history or infection. For odor signatures, the differences between individuals or clans are the message. The odor identity of the stud male mouse in the Bruce effect, in which the odor of a new male causes spontaneous abortion or reabsorption of the embryo in the female, is remembered by neuronal circuits in the accessory olfactory lobe after stimulation via the vomeronasal organ. In contrast, in the female sheep, the odor identity of her lamb is remembered in the main olfactory lobe. An important feature of odor signatures is that, unlike species-specific pheromones, odor signatures all have to be learned – in mammals, for example, by growing up with litter mates (which are later recognized as kin – and avoided as mates when adult). The importance of learning is demonstrated by cross-fostering experiments, which show a sensitive period of imprinting in the life of many young mammals. In ants, the colony identity odor has to be gained from fellow ants in the colony and learned on emergence from the pupa.
Production of Pheromones Pheromones are secreted by a variety of specialized glands in insects and mammals. In the same way that compounds become coopted as pheromones, glands are found in many different places in animals, usually as adapted skin glands. In mammals these occur in species-specific locations, for example near the eye, around the anus, or on the chin or flanks. Some pheromones are
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produced by internal organs; for example, the male sex pheromones of the sea lamprey, Petromyzon marinus, are bile acids produced by the liver. In a minority of species, the chemicals used for pheromone communication are collected. For example, male tropical euglossine bees must collect perfume compounds from orchid flowers to use as their sex pheromone. Some butterflies and moths – either as larvae or as adults – sequester plant poisons, and these may be adapted as sex pheromones in courtship (see the section titled ‘Sex pheromones’). Bark beetle pheromones may include compounds ingested from the tree sap and then chemically modified by the beetle itself or by symbiotic bacteria in the beetle’s gut. Pheromones (or signature odors) are produced by bacterial and fungal fermentation of fatty acids and other compounds secreted in the anal glands of dogs, badgers, and other carnivores.
Range of Roles for Chemical Communication Pheromones are used for a wide range of functions by animals. As might be expected, they are used especially by nocturnal species. Pheromone signals may be combined with other modalities – for example, on detecting a predator, black-tailed deer signal alarm with both a pheromone and a visual tail-flick signal. Pheromones can be classified by their apparent uses or functions – though a given pheromone can have more than one role in a species, depending on context.
Sex Pheromones The first pheromones identified were the sex pheromones of moths. It had long been known that male moths could find females at night; pheromones proved to be the means. At first each moth species was thought to have its own single unique compound as its pheromone. As more moth species were investigated, it was discovered that instead, each species had a unique blend of compounds as its pheromone. Different populations of the same species may have subtle variations of the blend, rather like a dialect. Goldfish sex pheromones have already been mentioned. Pheromones can be the subject of sexual selection. Pheromones may give clues to the status or quality of the pheromone emitter. For example, in many rodents, only high-ranking individuals, with high testosterone titers, will produce the male pheromones. In some moths which sequester plant poisons for defense, male pheromones are derived from their chemical store in a way which offers an honest signal of the quantity of defensive plant poison he will transfer to the female at mating.
Territorial Pheromones A key use of chemical communication by terrestrial vertebrates is for the marking of territories. An advantage of pheromones is that they can ‘shout’ ownership when the owner is not in that part of the territory. Male house mice mark their territories extensively with urine streaks. In the house mouse, only the dominant male will mark, and he defends this privilege vigorously should a subordinate male be rash enough to mark in the territory of the dominant male. Scrub-living antelopes mark their territories with orbital-gland pheromones, smearing secretions from the gland onto twigs at antelope head height. Some lizards mark their territories with leg gland secretions which have a double signal – a visual one (in the ultraviolet range, which lizards can see) to make it conspicuous from a distance and a volatile chemical signal detectable at close range.
Alarm Pheromones Alarm pheromones offer a warning or a call for help and marshal attack. Social insects – ants, bees, wasps, and the unrelated termites, all show colony defense coordinated by alarm pheromones. Honeybees release an alarm pheromone when they sting an intruder such as a bear intent on robbing their nest of its honey. The alarm pheromone attracts other bees from the nest to join in the attack. This collective defense can be very effective. The evolution of alarm pheromones is relatively straightforward to understand in social insects or other animals living in kin groups. However, what were previously called ‘alarm pheromones’ in fish are now called ‘alarm cues,’ as such fish live in groups of unrelated animals and thus it is hard to see how a signal could evolve to benefit the sender (the alarmed recipients of the cue are not related to the sender).
Aggregation Pheromones Some animals use pheromones to attract conspecifics. Bark beetles arriving on a tree use aggregation pheromones to attract the critical number of conspecifics needed to overwhelm the tree’s defenses. There is an optimum population density for the beetles, below which the beetles do less well – an Allee effect. As beetle density gets greater than the optimum, the pheromone messages released change, and potential settlers are deterred and go to other trees instead. Many marine animals such as barnacles respond to conspecific chemical cues to select the place to make their once-in-a-lifetime metamorphosis from planktonic larva to sessile adult glued to a rock. The presence of proteins left by adult barnacles indicates that
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the place is a good one to settle because members of that species have survived to maturity. It also ensures there will be other conspecific barnacles within reach for mating, which is important as these animals fertilize internally. Externally fertilizing marine animals coordinate density in time as well as space by using pheromones for a chemical duet between males and females which ensures that both sexes release their eggs and sperm into the water at the same time and in the same place. Some of the most spectacular examples come from marine polychaete worms, which spawn in enormous numbers on particular nights, all coordinated by pheromones.
Eavesdropping and Propaganda Broadcast signals can be ‘overheard’ or eavesdropped. This happens to pheromone communication too. Bark beetle pheromones are intended for other conspecifics, but predators have evolved great sensitivity to these compounds and can use them as kairomones to home in on calling bark beetles. Parasitic wasps can use the female moth’s pheromones to track down the moths whose eggs they parasitize. Some species of ant which take over the nests of other ant species use pheromones as allomones (‘propaganda’), releasing large quantities of the alarm pheromone of their victim species. This causes the victim species to run about chaotically but leaves the invading species unaffected. Bolas spiders and some orchids independently show some of the most spectacular uses of allomones to manipulate other species: bolas spiders synthesize the female sex pheromones used by moths and thereby lure male moths to their death. A single spider may produce the pheromones of different moth species over the course of an evening to match the flight times of those species. Orchids similarly synthesize female bee pheromones to attract male bees – though in this case the deception is for pollination, not to catch prey. Male bees attracted by the apparently authentic pheromone, mistaking it for a female bee, attempt to mate with the orchid flower, pick up pollen, and then fly on to be fooled again, delivering the pollen to another flower of the same orchid species.
Techniques for Studying Chemical Communication Chemical communication has proved more difficult than other modalities to study. The first reason is conceptual – our own worlds are so visual and auditory that we find it difficult to imagine the central role of chemical communication in the lives of most other organisms. The second has to do with the difficulties of chemical analysis. Much chemical communication uses vanishingly small quantities of chemical released by the signaler and perceived, at very low concentration, by the receiver of the signal. The quantities can stretch the limits of human instruments for detection (often we can detect the signal only by using the output from the animal’s own sense organs – as used in the electroantennogram, an electronic recording made from the antenna of a moth in response to chemical signals). The third challenge is the ‘playback’ of chemical signals. Organisms are very sensitive to precise molecular shapes of pheromones – the chirality of molecules has to be correct. This presents real challenges to the skills of synthetic chemists. In contrast to studies of communication by sound, there is no equivalent for pheromones of simple playback of a signal from a tape recorder or a computer-generated artificial signal. Apart from recordings from the sense organs of animals, a key requirement in the identification of molecules used for chemical communication is a bioassay. This can be behavioral, such as testing whether the candidate molecules elicit the same behavior as the putative pheromone. In testing potential pig sex pheromones, for example, the bioassay could be the lordosis (back arching and presentation behavior of the female pig) given in the presence of odors of the male pig (boar). Or the bioassay could be a physiological one, such as the quantity of semen produced by a male fish after exposure to putative female sex pheromones. Techniques for visualizing brain activity are gaining ground as tools to investigate the processing of chemical communication. Fluorescing dyes stimulated by free calcium concentrations have been used to investigate brain activity in response to odors in a variety of animals, including honeybees, salamanders, and zebrafish. Brain imaging using functional magnetic resonance imaging or positron-emission tomography has been used by researchers investigating chemical communication in vertebrates.
Exploiting Chemical Communication for Agriculture and Medicine The importance of chemical communication in the lives of animals offers many opportunities for applied use in agriculture, forestry, and, potentially, medicine. These uses are now well established for insect pest control, but with a few exceptions, their use with vertebrates is only just beginning. Mating disruption of pest moths in apple orchards by the release of synthetic female sex pheromone provides successful control of codling moth Cydia pomonella and other important pests of fruit. The synthetic pheromones seem to prevent males’ and females’ finding each other, so the females’ eggs are not fertilized – and no caterpillars result. Pheromones are particularly useful where
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pesticide resistance has developed, as has occurred for many pests of cotton. Pheromones provide a way to get off the ‘pesticide treadmill,’ in which farmers find they have to use additional pesticides to control previously innocuous insects which become pests when their predators are killed by the earlier rounds of pesticides. The specificity of pheromones means that very small quantities can be used and that non-target species are not affected. Unlike pesticides, pheromones leave predators unharmed, so these methods are compatible with biological control measures. Pest vertebrates too might be controlled by pheromones. The sea lamprey P. marinus has ravaged the Great Lakes fisheries in North America. Two lamprey pheromones, the male sex pheromone and the larval pheromone, are being explored to see whether they could be used to reduce lamprey populations by selective trapping or diversion. Mice and other pest rodents use pheromones for communication, and in the much longer term these perhaps could be used to control them. An understanding of pheromone priming effects could be useful in animal husbandry to, for example, advance puberty and reduce the postpartum period in pigs, and end seasonal anestrus in sheep and goats. Artificial insemination requires knowledge of when estrus is about to occur – the predictive lordosis response of the female pig is more reliable if they are sprayed with synthetic male pheromone (5a-androstenone, Boar Mate). Fish priming pheromones could be used in aquaculture to replace the individual hormone injections given to male fish to stimulate sperm production before semen collection. Pheromones may have a role to play in the future control of insect vectors of human diseases, such as the bloodsucking reduviid insects which carry Chagas disease. Nematodes, many of which cause human disease, use pheromones for communication, which might provide a route to control.
Do Humans Have Pheromones? There has been much speculation that two steroids, androstadienone (AND) and estratetraenol (EST) are male and female human pheromones, respectively. However, no robust evidence that these are human pheromones has ever been published. The claims can be traced back to a corporation in the 1990s and the positive results in the literature are sadly likely to be false positives. It is possible nonetheless that humans do have pheromones but the one nearest chemical identification is a potential mammary pheromone, seemingly released by glands around the nipple of lactating mothers. The secretion stimulates suckling by human babies, irrespective of which mother provided the secretion (ruling out a response due to individual recognition of the baby’s own mother).
Conclusions We are at an early stage in the investigation of chemical communication. Of all the senses, olfaction, because of the chemical communication it enables, is probably going to give us the most surprises in the future.
Further Reading Allison, J.D., Cardé, R.T. (Eds.), 2016. Pheromone Communication in Moths: Evolution, Behavior and Application. University of California Press, Berkeley, CA. Auer, T.O., Benton, R., 2016. Sexual circuitry in Drosophila. Curr. Opin. Neurobiol. 38, 18–26. Bear, D.M., Lassance, J.-M., Hoekstra, H.E., Datta, S.R., 2016. The evolving neural and genetic architecture of vertebrate olfaction. Curr. Biol. 26, R1039–R1049. Buchinger, T.J., Siefkes, M.J., Zielinski, B.S., Brant, C.O., Li, W., 2015. Chemical cues and pheromones in the sea lamprey (Petromyzon marinus). Front. Zool. 12, 32. Buettner, A. (ed.), 2017. Springer Handbook of Odor. Springer International Publishing, Cham. Carla, M.-C. (Ed.), 2014. Neurobiology of Chemical Communication. CRC Press, Boca Raton, FL. De Bruyne, M., Baker, T.C., 2008. Odor detection in insects: volatile codes. J. Chem. Ecol. 34, 882–897. Galizia, G., Lledo, P.M. (Eds.), 2013. Neurosciences – from Molecule to Behavior: A University Textbook. Springer, Berlin. Jorre De St Jorre, T., Hawken, P.A.R., Martin, G.B., 2014. New understanding of an old phenomenon: uncontrolled factors and misconceptions that cast a shadow over studies of the ‘male effect’ on reproduction in small ruminants. Turk. J. Vet. Anim. Sci. 38, 625–636. Leighton, D.H., Sternberg, P.W., 2016. Mating pheromones of Nematoda: olfactory signaling with physiological consequences. Curr. Opin. Neurobiol. 38, 119–124. Liberles, S.D., 2014. Mammalian pheromones. Annu. Rev. Physiol. 76, 151–175. Mucignat-Caretta, C., Redaelli, M., Caretta, A., 2012. One nose, one brain: contribution of the main and accessory olfactory system to chemosensation. Front. Neuroanat. 6, 46. Oi, C.A., Van Zweden, J.S., Oliveira, R.C., Van Oystaeyen, A., Nascimento, F.S., Wenseleers, T., 2015. The origin and evolution of social insect queen pheromones: novel hypotheses and outstanding problems. BioEssays 37, 808–821. Schulte, B.A., Goodwin, T.E., Ferkin, M.H. (Eds.), 2015. Chemical Signals in Vertebrates, vol. 13. Springer International Publishing, Cham. Sorensen, P.W., Wisenden, B.D. (Eds.), 2015. Fish Pheromones and Related Cues. John Wiley, Hoboken. Spehr, M., 2017. Olfactory subsystems. In: Buettner, A. (Ed.), Springer handbook of Odor. Springer International Publishing, Cham, p. 78. Touhara, K. (Ed.), 2013. Pheromone Signaling: Methods and Protocols. Humana Press (Springer), New York, NY. Witzgall, P., Kirsch, P., Cork, A., 2010. Sex pheromones and their impact on pest management. J. Chem. Ecol. 36, 80–100. Wyatt, T.D., 2010. Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 196, 685–700. q
Change History: March 2017. TD Wyatt updated all sections of the text and Further Reading and added Figure 1.
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Wyatt, T.D., 2014. Pheromones and Animal Behavior: Chemical Signals and Signatures, second ed. Cambridge University Press, Cambridge. Wyatt, T.D., 2015. The search for human pheromones: the lost decades and the necessity of returning to first principles. Proc. R. Soc. Lond. B Biol. Sci. 282 http://dx.doi.org/ 10.1098/rspb.2014.2994. Wyatt, T.D., 2017. Pheromones. Curr. Biol. 27, R1–R5. Zufall, F., Munger, S.D. (Eds.), 2016. Chemosensory Transduction: The Detection of Odors, Tastes, and Other Chemostimuli. Academic Press, London.
Relevant Website www.pherobase.com – The Pherobase: Database of Pheromones and Semiochemicals.
Introduction Evolution of Chemical Communication Mechanism of Olfaction, Receptor Proteins, and the Evolution of Pheromones Releaser and Primer Effects of Pheromones Odor Signatures Contrasted With Chemical Signals (Pheromones) Production of Pheromones Range of Roles for Chemical Communication Sex Pheromones Territorial Pheromones Alarm Pheromones Aggregation Pheromones Eavesdropping and Propaganda Techniques for Studying Chemical Communication Exploiting Chemical Communication for Agriculture and Medicine Do Humans Have Pheromones? Conclusions Further Reading Relevant Website
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Introduction Chemical communication is arguably the most widely shared sensory modality, used almost universally across the animal kingdom. From the simplest bacteria to humans, almost all organisms use chemical communication. Within a species, the molecules used for chemical signals are called pheromones. The word pheromone comes from the Greek pherein, to carry or transfer, and horman, to excite or stimulate. Pheromones are often divided by function, such as sex pheromones and aggregation pheromones. A broader term for chemicals involved in animal communication is semiochemical (from the Greek semeion, sign) (Fig. 1). Chemical signals broadcast to the world can also be detected by individuals from other species. So, for example, pheromones
Semiochemicals
Between members of different species
Between members of same species
Signature mixtures
Pheromones
Allelochemicals
species-wide signals
learned by receiver from highly variable chemical profile of conspecific
Allomones
Kairomones
Synomones
benefit emitter, of a different species
benefit receiver, of a different species
benefit both emitter & receiver, of different species
Figure 1 Pheromones are chemical signals used between members of the same species. Pheromones are the same in all sexually mature males, for example, of a species. Individual recognition relies instead on the learning of signature mixtures for individuals (for recognition of siblings for example), based on differences in chemical profile between individuals. Allelochemical is the term given to chemical information received by members of different species. Figure from Wyatt (2014), reprinted with permission from Cambridge University Press.
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released by bark beetles may attract their predators – which use the pheromones as a kairomone to locate their bark beetle prey. Chemical signals in deceit or propaganda are termed allomones (discussed in the section titled ‘Eavesdropping and propaganda’). The pheromones above are defined molecules or ratios of particular molecules. All males, for example, of a species produce the same molecules as pheromones, though dominant males may produce more than subordinates, as for example in mice.
Evolution of Chemical Communication Pheromones evolve from chemicals released to the environment that give an advantage to the receiver and the sender. The clue to such an evolutionary path is often given by the identity of the compounds used as pheromones. For example, the sex pheromones released by female goldfish appear to be very similar to the steroid hormones that are circulating in her blood while her eggs are developing. Male goldfish have evolved great sensitivity to these hormone-like compounds. Presumably, over evolutionary time, males able to detect these compounds, initially inadvertently leaking from females, would gain more fertilizations as they would be better able to find the females about to spawn. There would be selection for greater and greater sensitivity in the ‘noses’ of the males – to the extent that now male goldfish can detect the waterborne sex pheromones down to nanomolar and picomolar threshold concentrations. Females would gain more reliable fertilization, so there would be selection for females that, instead of simply leaking these compounds, actually secreted them. Thus, theoretically, something which started as eavesdropping by males could evolve into a pheromone signal produced by females specifically to attract males. Another example comes from the alarm pheromones in ants, released when threatened by a predator or invading ants from another colony. A bizarre variety of compounds are found as alarm pheromones in different taxonomic groups of ants. The pattern is largely explained when the alarm pheromones are compared with the toxic compounds that are released in fighting or defense in those species – the alarm pheromones appear, in many species, to have evolved from defense compounds. Thus all kinds of molecules can potentially evolve to become used as pheromones in chemical communication. The size and stability of compounds can often be related to their role in communication. For example, ant alarm pheromones tend to be small, volatile molecules which diffuse quickly. Hyena territorial marking pheromones are high-molecular- weight involatile compounds, which will last a long time. A wide variety of the compounds are used by different species as pheromones, including steroids, fatty acids, and esters. Some aquatic invertebrates and vertebrates, including amphibians, use short peptides as pheromones. For example, the Asian red-bellied newt (Cynops pyrrhogaster) uses a decapeptide, sodefrin, as its male sex pheromone. The sea slug mollusk Aplysia uses a combination of proteins as its sex pheromone. Small molecules as well as large ones are used by animals large and small. The mammary pheromone of the rabbit, 2-methylbut2-enal, stimulates suckling in rabbit pups. In mammals, some low-molecular-weight pheromones are delivered loosely in the cleft of a protein, which increases the longevity of the signal. For example, small molecule pheromones in the house mouse, such as dehydro-exo-brevicomin, are presented in association with lipocalin major urinary proteins (MUPs), increasing the life of the signal as the small molecules are slowly released. Large quantities of MUPs are present in the urine of dominant male mice. The MUPs may also give some individuality to the signal of the male. One of the MUPs, MUP20 (also known as darcin), is produced by all males and is a male pheromone. When a female mouse sniffs darcin into her vomeronasal organ (VNO) she remembers the location of the male’s scent mark and his individual small molecule odor profile. Some molecules are used as pheromones by unrelated species. For example, brevicomin is used as a pheromone by some bark beetles and dehydro-exo-brevicomin is used by male mice. Such a shared use is not unusual. The Asian elephant (Elephas maximus) shares its female sex pheromone with some 140 species of moth. The compound is a small, volatile molecule, (Z)-7-dodecen-1-yl acetate. This phenomenon comes about because of the common origin of life: basic enzyme pathways are common to all multicellular organisms. In addition, the number of potential different small, and thus volatile, molecules is limited by the number of permutations of combining a small number of atoms. However, moths and elephants are unlikely to be confused by each other as female elephants produce prodigious amounts of the pheromone (and the amounts produced by a female moth will not be noticed by a male elephant) and male moths are attracted to species-specific combinations of pheromone components, of which the elephant pheromone is just one. Most chemical communication, such as that of moths, is by mixtures of small molecules which give species specificity to messages. Female moths’ pheromones tend to consist of a species-specific combination of fatty acids or alcohols. Males respond to the whole blend as a signal. Unique compounds such as the complex molecule supellapyrone, used as a sex pheromone by the brown-banded cockroach, Supella longipalpa, are unusual. However, animals using peptides as their pheromones can have species-specific sequences: another Japanese newt species, Cynops ensicauda uses a decapeptide which differs by two amino acids from the male sex pheromone, sodefrin, of its sister species C. pyrrhogaster. In moths we can see speciation reflected in their chemical communication. Related species may have similar pheromone blends, distinguished by different proportions of the compounds or the addition or loss of certain components. In some moth families, the synthetic pathways for the pheromone blend components are well understood. With this background, the variation in blends produced by different species can be explained by gene frequency changes and mutations, resulting in up- or downregulation of particular enzymes or changes in reaction product or substrate. There may be regional variation in pheromone blends within a moth species, and incipient speciation can sometimes be observed.
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Mechanism of Olfaction, Receptor Proteins, and the Evolution of Pheromones In animals with an olfactory system, with few exceptions pheromones are detected by the olfactory system rather than the gustatory system. The organization of the olfactory system in invertebrates and vertebrates is remarkably similar in functional terms. The great flexibility of the olfactory system means that almost any kind of chemical can potentially evolve into a pheromone if it provides useful information to the receiver. This is because olfaction works by stimulation of a wide range of relatively nonspecific receptor proteins (each expressed on different olfactory sensory neurons linked to glomeruli). The system can respond to the widest possible range of odors, even as entirely new compounds are created (in evolving biological systems). Although a given odor may be unlikely to fit any one receptor perfectly, it is likely to stimulate some. If detection of a molecule gives significant selective advantage, then over evolutionary time, the receptors may evolve great specificity to such molecules; so, for example, on the male moth antennae there are large banks of thousands of olfactory sensory neurons, each with a receptor type very finely tuned to one of the key components of that species’ female sex pheromone. Many vertebrates have a second olfactory system, the vomeronasal organ (VNO), which projects to the accessory olfactory lobe, as well as the main olfactory system. Depending on species, pheromones are detected by either the main olfactory system or the vomeronasal organ or, as seems increasingly likely, both systems. Projections from both systems converge on the amygdala, enabling extensive integration of their chemosensory inputs. Outputs from the medial amygdala lead to pheromone primer effects by activating particular neurons in the hypothalamus.
Releaser and Primer Effects of Pheromones The first pheromones recognized were sex pheromones which elicited (or ‘released’) an almost instantaneous behavioral response. For example, in moths, female sex pheromones elicit orientation flights by males toward the female, and when he finds her, in many species, the male fans his wings as part of courtship. This formed the bioassay used to identify the pheromone (see the section titled ‘Techniques for studying chemical communication’). Some pheromones produce longer-term physiological changes (primer effects) in the receiver. For example, the female goldfish sex pheromones, besides attracting males, also cause the receiving males to increase their sperm and semen production. Primer effects act via the receiver’s endocrine system. There are many interactions between pheromones and the central and the peripheral nervous systems and endocrine systems. Some primer effects can be rapid, and the effects of some behavioral interactions mediated by pheromones can be long lasting. In social insects, queen pheromones with primer effects have been chemically identified in recent years, first in ants then in wasps and bees. These pheromones, independently evolved in each lineage, are produced by the queen in a social insect colony and signal to workers that she is fertile and laying eggs. The reproductive system of the workers is shut down in the presence of queen pheromone. A further class of pheromones, allohormone pheromones, bypass the usual olfactory system of the recipient. A honeybee egg can develop into a worker or a queen. What determines its development is what the larva is fed. If it is fed exclusively with royal jelly, then the genes appropriate for development into a queen are activated. The allohormone pheromone in the royal jelly may include a protein called royalactin which acts on cells in the fat body of the developing larva.
Odor Signatures Contrasted With Chemical Signals (Pheromones) Rather different from pheromones are ‘odor signatures’ which differ between individuals or family groups (or, in social insects, colonies) of the same species. This variability in odor signature makes recognition of individuals or families possible by smell. The odor signature is very complex and is made up from all sources of variation, both genetic and environmental, including recent feeding history or infection. For odor signatures, the differences between individuals or clans are the message. The odor identity of the stud male mouse in the Bruce effect, in which the odor of a new male causes spontaneous abortion or reabsorption of the embryo in the female, is remembered by neuronal circuits in the accessory olfactory lobe after stimulation via the vomeronasal organ. In contrast, in the female sheep, the odor identity of her lamb is remembered in the main olfactory lobe. An important feature of odor signatures is that, unlike species-specific pheromones, odor signatures all have to be learned – in mammals, for example, by growing up with litter mates (which are later recognized as kin – and avoided as mates when adult). The importance of learning is demonstrated by cross-fostering experiments, which show a sensitive period of imprinting in the life of many young mammals. In ants, the colony identity odor has to be gained from fellow ants in the colony and learned on emergence from the pupa.
Production of Pheromones Pheromones are secreted by a variety of specialized glands in insects and mammals. In the same way that compounds become coopted as pheromones, glands are found in many different places in animals, usually as adapted skin glands. In mammals these occur in species-specific locations, for example near the eye, around the anus, or on the chin or flanks. Some pheromones are
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produced by internal organs; for example, the male sex pheromones of the sea lamprey, Petromyzon marinus, are bile acids produced by the liver. In a minority of species, the chemicals used for pheromone communication are collected. For example, male tropical euglossine bees must collect perfume compounds from orchid flowers to use as their sex pheromone. Some butterflies and moths – either as larvae or as adults – sequester plant poisons, and these may be adapted as sex pheromones in courtship (see the section titled ‘Sex pheromones’). Bark beetle pheromones may include compounds ingested from the tree sap and then chemically modified by the beetle itself or by symbiotic bacteria in the beetle’s gut. Pheromones (or signature odors) are produced by bacterial and fungal fermentation of fatty acids and other compounds secreted in the anal glands of dogs, badgers, and other carnivores.
Range of Roles for Chemical Communication Pheromones are used for a wide range of functions by animals. As might be expected, they are used especially by nocturnal species. Pheromone signals may be combined with other modalities – for example, on detecting a predator, black-tailed deer signal alarm with both a pheromone and a visual tail-flick signal. Pheromones can be classified by their apparent uses or functions – though a given pheromone can have more than one role in a species, depending on context.
Sex Pheromones The first pheromones identified were the sex pheromones of moths. It had long been known that male moths could find females at night; pheromones proved to be the means. At first each moth species was thought to have its own single unique compound as its pheromone. As more moth species were investigated, it was discovered that instead, each species had a unique blend of compounds as its pheromone. Different populations of the same species may have subtle variations of the blend, rather like a dialect. Goldfish sex pheromones have already been mentioned. Pheromones can be the subject of sexual selection. Pheromones may give clues to the status or quality of the pheromone emitter. For example, in many rodents, only high-ranking individuals, with high testosterone titers, will produce the male pheromones. In some moths which sequester plant poisons for defense, male pheromones are derived from their chemical store in a way which offers an honest signal of the quantity of defensive plant poison he will transfer to the female at mating.
Territorial Pheromones A key use of chemical communication by terrestrial vertebrates is for the marking of territories. An advantage of pheromones is that they can ‘shout’ ownership when the owner is not in that part of the territory. Male house mice mark their territories extensively with urine streaks. In the house mouse, only the dominant male will mark, and he defends this privilege vigorously should a subordinate male be rash enough to mark in the territory of the dominant male. Scrub-living antelopes mark their territories with orbital-gland pheromones, smearing secretions from the gland onto twigs at antelope head height. Some lizards mark their territories with leg gland secretions which have a double signal – a visual one (in the ultraviolet range, which lizards can see) to make it conspicuous from a distance and a volatile chemical signal detectable at close range.
Alarm Pheromones Alarm pheromones offer a warning or a call for help and marshal attack. Social insects – ants, bees, wasps, and the unrelated termites, all show colony defense coordinated by alarm pheromones. Honeybees release an alarm pheromone when they sting an intruder such as a bear intent on robbing their nest of its honey. The alarm pheromone attracts other bees from the nest to join in the attack. This collective defense can be very effective. The evolution of alarm pheromones is relatively straightforward to understand in social insects or other animals living in kin groups. However, what were previously called ‘alarm pheromones’ in fish are now called ‘alarm cues,’ as such fish live in groups of unrelated animals and thus it is hard to see how a signal could evolve to benefit the sender (the alarmed recipients of the cue are not related to the sender).
Aggregation Pheromones Some animals use pheromones to attract conspecifics. Bark beetles arriving on a tree use aggregation pheromones to attract the critical number of conspecifics needed to overwhelm the tree’s defenses. There is an optimum population density for the beetles, below which the beetles do less well – an Allee effect. As beetle density gets greater than the optimum, the pheromone messages released change, and potential settlers are deterred and go to other trees instead. Many marine animals such as barnacles respond to conspecific chemical cues to select the place to make their once-in-a-lifetime metamorphosis from planktonic larva to sessile adult glued to a rock. The presence of proteins left by adult barnacles indicates that
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the place is a good one to settle because members of that species have survived to maturity. It also ensures there will be other conspecific barnacles within reach for mating, which is important as these animals fertilize internally. Externally fertilizing marine animals coordinate density in time as well as space by using pheromones for a chemical duet between males and females which ensures that both sexes release their eggs and sperm into the water at the same time and in the same place. Some of the most spectacular examples come from marine polychaete worms, which spawn in enormous numbers on particular nights, all coordinated by pheromones.
Eavesdropping and Propaganda Broadcast signals can be ‘overheard’ or eavesdropped. This happens to pheromone communication too. Bark beetle pheromones are intended for other conspecifics, but predators have evolved great sensitivity to these compounds and can use them as kairomones to home in on calling bark beetles. Parasitic wasps can use the female moth’s pheromones to track down the moths whose eggs they parasitize. Some species of ant which take over the nests of other ant species use pheromones as allomones (‘propaganda’), releasing large quantities of the alarm pheromone of their victim species. This causes the victim species to run about chaotically but leaves the invading species unaffected. Bolas spiders and some orchids independently show some of the most spectacular uses of allomones to manipulate other species: bolas spiders synthesize the female sex pheromones used by moths and thereby lure male moths to their death. A single spider may produce the pheromones of different moth species over the course of an evening to match the flight times of those species. Orchids similarly synthesize female bee pheromones to attract male bees – though in this case the deception is for pollination, not to catch prey. Male bees attracted by the apparently authentic pheromone, mistaking it for a female bee, attempt to mate with the orchid flower, pick up pollen, and then fly on to be fooled again, delivering the pollen to another flower of the same orchid species.
Techniques for Studying Chemical Communication Chemical communication has proved more difficult than other modalities to study. The first reason is conceptual – our own worlds are so visual and auditory that we find it difficult to imagine the central role of chemical communication in the lives of most other organisms. The second has to do with the difficulties of chemical analysis. Much chemical communication uses vanishingly small quantities of chemical released by the signaler and perceived, at very low concentration, by the receiver of the signal. The quantities can stretch the limits of human instruments for detection (often we can detect the signal only by using the output from the animal’s own sense organs – as used in the electroantennogram, an electronic recording made from the antenna of a moth in response to chemical signals). The third challenge is the ‘playback’ of chemical signals. Organisms are very sensitive to precise molecular shapes of pheromones – the chirality of molecules has to be correct. This presents real challenges to the skills of synthetic chemists. In contrast to studies of communication by sound, there is no equivalent for pheromones of simple playback of a signal from a tape recorder or a computer-generated artificial signal. Apart from recordings from the sense organs of animals, a key requirement in the identification of molecules used for chemical communication is a bioassay. This can be behavioral, such as testing whether the candidate molecules elicit the same behavior as the putative pheromone. In testing potential pig sex pheromones, for example, the bioassay could be the lordosis (back arching and presentation behavior of the female pig) given in the presence of odors of the male pig (boar). Or the bioassay could be a physiological one, such as the quantity of semen produced by a male fish after exposure to putative female sex pheromones. Techniques for visualizing brain activity are gaining ground as tools to investigate the processing of chemical communication. Fluorescing dyes stimulated by free calcium concentrations have been used to investigate brain activity in response to odors in a variety of animals, including honeybees, salamanders, and zebrafish. Brain imaging using functional magnetic resonance imaging or positron-emission tomography has been used by researchers investigating chemical communication in vertebrates.
Exploiting Chemical Communication for Agriculture and Medicine The importance of chemical communication in the lives of animals offers many opportunities for applied use in agriculture, forestry, and, potentially, medicine. These uses are now well established for insect pest control, but with a few exceptions, their use with vertebrates is only just beginning. Mating disruption of pest moths in apple orchards by the release of synthetic female sex pheromone provides successful control of codling moth Cydia pomonella and other important pests of fruit. The synthetic pheromones seem to prevent males’ and females’ finding each other, so the females’ eggs are not fertilized – and no caterpillars result. Pheromones are particularly useful where
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pesticide resistance has developed, as has occurred for many pests of cotton. Pheromones provide a way to get off the ‘pesticide treadmill,’ in which farmers find they have to use additional pesticides to control previously innocuous insects which become pests when their predators are killed by the earlier rounds of pesticides. The specificity of pheromones means that very small quantities can be used and that non-target species are not affected. Unlike pesticides, pheromones leave predators unharmed, so these methods are compatible with biological control measures. Pest vertebrates too might be controlled by pheromones. The sea lamprey P. marinus has ravaged the Great Lakes fisheries in North America. Two lamprey pheromones, the male sex pheromone and the larval pheromone, are being explored to see whether they could be used to reduce lamprey populations by selective trapping or diversion. Mice and other pest rodents use pheromones for communication, and in the much longer term these perhaps could be used to control them. An understanding of pheromone priming effects could be useful in animal husbandry to, for example, advance puberty and reduce the postpartum period in pigs, and end seasonal anestrus in sheep and goats. Artificial insemination requires knowledge of when estrus is about to occur – the predictive lordosis response of the female pig is more reliable if they are sprayed with synthetic male pheromone (5a-androstenone, Boar Mate). Fish priming pheromones could be used in aquaculture to replace the individual hormone injections given to male fish to stimulate sperm production before semen collection. Pheromones may have a role to play in the future control of insect vectors of human diseases, such as the bloodsucking reduviid insects which carry Chagas disease. Nematodes, many of which cause human disease, use pheromones for communication, which might provide a route to control.
Do Humans Have Pheromones? There has been much speculation that two steroids, androstadienone (AND) and estratetraenol (EST) are male and female human pheromones, respectively. However, no robust evidence that these are human pheromones has ever been published. The claims can be traced back to a corporation in the 1990s and the positive results in the literature are sadly likely to be false positives. It is possible nonetheless that humans do have pheromones but the one nearest chemical identification is a potential mammary pheromone, seemingly released by glands around the nipple of lactating mothers. The secretion stimulates suckling by human babies, irrespective of which mother provided the secretion (ruling out a response due to individual recognition of the baby’s own mother).
Conclusions We are at an early stage in the investigation of chemical communication. Of all the senses, olfaction, because of the chemical communication it enables, is probably going to give us the most surprises in the future.
Further Reading Allison, J.D., Cardé, R.T. (Eds.), 2016. Pheromone Communication in Moths: Evolution, Behavior and Application. University of California Press, Berkeley, CA. Auer, T.O., Benton, R., 2016. Sexual circuitry in Drosophila. Curr. Opin. Neurobiol. 38, 18–26. Bear, D.M., Lassance, J.-M., Hoekstra, H.E., Datta, S.R., 2016. The evolving neural and genetic architecture of vertebrate olfaction. Curr. Biol. 26, R1039–R1049. Buchinger, T.J., Siefkes, M.J., Zielinski, B.S., Brant, C.O., Li, W., 2015. Chemical cues and pheromones in the sea lamprey (Petromyzon marinus). Front. Zool. 12, 32. Buettner, A. (ed.), 2017. Springer Handbook of Odor. Springer International Publishing, Cham. Carla, M.-C. (Ed.), 2014. Neurobiology of Chemical Communication. CRC Press, Boca Raton, FL. De Bruyne, M., Baker, T.C., 2008. Odor detection in insects: volatile codes. J. Chem. Ecol. 34, 882–897. Galizia, G., Lledo, P.M. (Eds.), 2013. Neurosciences – from Molecule to Behavior: A University Textbook. Springer, Berlin. Jorre De St Jorre, T., Hawken, P.A.R., Martin, G.B., 2014. New understanding of an old phenomenon: uncontrolled factors and misconceptions that cast a shadow over studies of the ‘male effect’ on reproduction in small ruminants. Turk. J. Vet. Anim. Sci. 38, 625–636. Leighton, D.H., Sternberg, P.W., 2016. Mating pheromones of Nematoda: olfactory signaling with physiological consequences. Curr. Opin. Neurobiol. 38, 119–124. Liberles, S.D., 2014. Mammalian pheromones. Annu. Rev. Physiol. 76, 151–175. Mucignat-Caretta, C., Redaelli, M., Caretta, A., 2012. One nose, one brain: contribution of the main and accessory olfactory system to chemosensation. Front. Neuroanat. 6, 46. Oi, C.A., Van Zweden, J.S., Oliveira, R.C., Van Oystaeyen, A., Nascimento, F.S., Wenseleers, T., 2015. The origin and evolution of social insect queen pheromones: novel hypotheses and outstanding problems. BioEssays 37, 808–821. Schulte, B.A., Goodwin, T.E., Ferkin, M.H. (Eds.), 2015. Chemical Signals in Vertebrates, vol. 13. Springer International Publishing, Cham. Sorensen, P.W., Wisenden, B.D. (Eds.), 2015. Fish Pheromones and Related Cues. John Wiley, Hoboken. Spehr, M., 2017. Olfactory subsystems. In: Buettner, A. (Ed.), Springer handbook of Odor. Springer International Publishing, Cham, p. 78. Touhara, K. (Ed.), 2013. Pheromone Signaling: Methods and Protocols. Humana Press (Springer), New York, NY. Witzgall, P., Kirsch, P., Cork, A., 2010. Sex pheromones and their impact on pest management. J. Chem. Ecol. 36, 80–100. Wyatt, T.D., 2010. Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 196, 685–700. q
Change History: March 2017. TD Wyatt updated all sections of the text and Further Reading and added Figure 1.
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Wyatt, T.D., 2014. Pheromones and Animal Behavior: Chemical Signals and Signatures, second ed. Cambridge University Press, Cambridge. Wyatt, T.D., 2015. The search for human pheromones: the lost decades and the necessity of returning to first principles. Proc. R. Soc. Lond. B Biol. Sci. 282 http://dx.doi.org/ 10.1098/rspb.2014.2994. Wyatt, T.D., 2017. Pheromones. Curr. Biol. 27, R1–R5. Zufall, F., Munger, S.D. (Eds.), 2016. Chemosensory Transduction: The Detection of Odors, Tastes, and Other Chemostimuli. Academic Press, London.
Relevant Website www.pherobase.com – The Pherobase: Database of Pheromones and Semiochemicals.