ISSN 1062-3590, Biology Bulletin, 2016, Vol. 43, No. 9, pp. 1175–1183. © Pleiades Publishing, Inc., 2016. Original Russian Text © A.V. Surov, A.N. Maltsev, 2016, published in Zoologicheskii Zhurnal, 2016, Vol. 95, No. 12, pp. 1449–1458.
This review was published in honor of the centenary of Zoologicheskii Zhurnal
Analysis of Chemical Communication in Mammals: Zoological and Ecological Aspects A. V. Surov* and A. N. Maltsev Severtsov Institute for Problems of Ecology and Evolution, Russian Academy of Sciences, Moscow 119071, Russia *e-mail:
[email protected] Received June 7, 2016
Abstract⎯Chemical communication is one of the most important branches of zoology and chemical ecology. In the review, we analyze the main directions of chemical communication in mammals, mainly as based on the works of Russian researchers belonging to the school of the late Academician V.E. Sokolov, some approaches to solving specific zoological and ecological problems, and future prospects of the development of research. The following areas of research are discussed: the role of chemical signals as reproductive isolating mechanisms, sex pheromones, the recognition of individual odor, a seasonal hormonal response to olfactory signals, and the chemistry of natural substances. Keywords: chemical communication, mammals, pheromones DOI: 10.1134/S1062359016110157
Chemical sense is the most ancient sense found in all living organisms starting from bacteria. Therefore, animals are preadapted to the perception of various chemical signals from the environment (Wilson, 1970). The range of its use is very wide: marking of territory, search for food and sexual partner, stimulation of sexual behavior, recognition of species and sex, control of aggressive interactions, etc. The organs that allow perception of both volatile and non-volatile chemicals have passed a long way of evolution. In primitive organisms, responses to chemicals are ensured by specialized cells, whereas in higher vertebrates they are ensured by highly organized olfactory organs. The complexity of the receptor apparatus increased simultaneously with the improvement of the methods of processing of incoming information. Olfactory brain centers have served as the basis for subsequent formation of correlative and associative mechanisms of higher nervous activity in terrestrial vertebrates (Romer and Parsons, 1992). If the perception of a specific chemical signal increases the reproductive success or survival, selection is aimed at reducing the threshold of sensitivity to this substance and/or at increasing the expression of the genes responsible for its perception. Animals are able to “fine-tune” their olfactory system through the formation of specialized organs and relationships in the central nervous system (Wyatt, 2003).
According to the concept formulated by Naumov in the 1970s (Naumov, 1973, 1977), chemical communication can be considered as an integral part of the biological signaling field. Apparently, the chemical signals, as part of biological signal field, provide the regulation of physiological processes, including reproduction, recognition, and adjustment of behavioral responses of individuals to each other. Systematic studies of chemical communication in mammals in Russia began in the 1970s under the supervision of Academician V.E. Sokolov. It was he who, being an expert in the morphology of skin glands of mammals, recruited a number of experts to study the communicative functions of these structures and then other excreta. For many years, this has determined the direction of research in this field in Russia. Researchers headed by Sokolov have started and continue today to investigate the morphology of specific skin glands (Sokolov and Chernova, 2001; Stepanova, 1998) and their functions (Vasilieva and Sokolov, 1994; Bodyak, 1994), mediated communication of mammals (Rozhnov, 2011), the role of chemical signals as isolating reproductive barriers (Kotenkova, 2014), sex pheromones of mammals (Surov, 2006), the effect of odor of a predator on the reproduction of rodents (Voznessenskaya, 2014), seasonal hormonal response to olfactory signals (Feoktistova and Naidenko, 2006), and chemistry of natural substances
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(Zinkevich and Vasil’eva, 1998; Zinkevich, 2003). A significant contribution to the research of chemical communication of animal was made by the studies under the All-Union Research Program for Studies of Pheromones and Chemical Communication of Animals, which was proposed by V.E. Sokolov in 1979 and which united the work of hundreds of local scientists. The implementation of this program was reflected in numerous publications, including the Zoologicheskii Zhurnal. Regular All-Union and then Russia conferences, collected papers (Pheromones and Behavior, Moscow, 1982; Chemical Signals of Animals, Moscow, 1982; Signaling and Ecology of Mammals and Birds, Moscow, 1984; Chemical Communication of Animals, Moscow, 1986; Relevant Problems of Morphology and Ecology of Higher Vertebrates, Moscow, 1988; Chemical Communication of Animals: Fundamental Problems, Moscow, 2006; etc.) comprehensively reflected the research of chemical communication of invertebrates and vertebrates as well as the research of olfaction mechanisms. In late 1960s, an assumption was made that chemical signals play a crucial role in the formation of reproductive isolation between closely related taxa, which was based on the hypothesis of the existence of a species-specific odor. The role of chemical signals in the pre-copulatory mechanisms in closely related species of house mice of the superspecies complex Mus musculus s. l. was started under the supervision of V.E. Sokolov. It was shown that both sympatric and allopatric species of mice readily recognize individuals of their own and closely related species by the odor of urine and longer explore the source of odor of conspecific at a pairwise presentation with non-conspecific (Kotenkova et al., 1989; Sokolov et al., 1990; Kotenkova and Naidenko, 1999; Maltsev and Kotenkova, 2013). It was shown that only the odor of an estrous female of the own, but not a closely related, species of mice activated the receptors of the vomeronasal organ and the corresponding projection area of the auxiliary olfactory bulb (Voznessenskaya et al., 2010). The results of these and other studies made it possible to propose and substantiate the action of the precopulatory isolating mechanisms in sympatric (i.e., reliably isolated in nature) closely related species of house mice (Kotenkova, 2014). In studying the responses to odors among the representatives of two chromosome races Microtus arvalis arvalis and M. a. obscurus, it was found that they readily recognize the representatives of their own race by odor and distinguish them from the representative of the another chromosome form (Meyer et al., 2000). Such examples are quite numerous (Kotenkova, 2014). However, to answer the question about the role of the genetic component in the formation of responses to the own form during ontogeny, special studies are required. The studies of chemical communication are inextricably associated with the term “pheromone.” Initially, this term was used for “substances which are
secreted to the outside by an individual and received by a second individual of the same species, in which they release a specific reaction, for example, a definite behaviour or a developmental process” (Karlson and Lusher, 1959). In the last 50 years that have passed since the discovery of the first sex hormone, bombykol (Butenandt et al., 1959), considerable progress was made in decoding and synthesis of insect pheromones. Sex pheromones of hundreds of insect species have been isolated, identified, and synthesized. The majority of them are successfully used against agricultural pests, which is reflected in the regularly updated database of insect pheromones and other biologically active substances (El-Sayed, 2014). However, in insects, the situation when one substance causes a specific response is also observed rather rarely. To promote a specific behavioral response of an insect (especially of social species), a mixture of chemical substances is required, and the response itself depends on many factors (learning, physiological state, etc.) (Holldobler, 1999). The situation with the chemical signals of mammals is even more intricate. Virtually none of the mammalian pheromones has been decoded so far in that context that had been initially assigned to this term. The biological activity of many substances that were regarded as mammalian pheromones was not confirmed later. This happened, for example, with the sexual receptivity pheromone of the rhesus monkey (Michael and Keverne, 1968), the aphrodisiac protein of the Syrian hamster (Singer et al., 1986), and the substances that signal the estrus of bitchs (Goodwin et al., 1979). A number of laboratory effects were described that can be interpreted as the result of the action of pheromones: pregnancy blocking by the odor of another male (Bruce, 1959), accelerated maturation of females under the influence of male odor (Vandenbergh, 1983), synchronization of estrous cycles of females in the presence of male odor (Whitten, 1966), etc. However, these effects were not confirmed under conditions close to natural (Wolff, 2003), and the specific substances responsible for these effects were not identified (Doty, 2010). The limited possibilities of using pheromones by mammals (in the narrow sense of the term) are associated with their higher level of biological organization, the existence of complex relationships between their behavioral and physiological responses, and a higher importance of situational scope as compared to other groups of animals (Doty, 2010). The response to chemical signals in mammals can be not only innate but may also depend on the experience obtained in ontogeny (Logan, 2015). The problems occurring in studying chemical communication can be caused not only by the complexity of organization of mammalian behavior but also by the methodological difficulties associated with the specifics of functioning of the olfactory system and the BIOLOGY BULLETIN
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nature of the chemical signal as such. (1) The thresholds of perception of many volatiles by the olfactory organ of mammals are usually much lower than in modern devices. In addition, gas analyzers are based on the principle of sequential information reading, whereas the olfactory organ simultaneously perceives all substances contained in a mixture (i.e., as a musical chord or a bouquet). (2) In contrast to the acoustic signals, which are set by a limited number of parameters (wavelength, amplitude, and phase), the olfactory signals, which are characterized by a large number of parameters (concentration, volatility, synergy, etc.), are more difficult to dose, record, and display (Bradbury and Vehrencamp, 2011). (3) The mechanism of functioning of olfactory receptors is studied insufficiently. It was recently found that thousands of types of receptor cells are involved in the perception of odoriferous molecules and that up to 3% of the genome is responsible for the synthesis of receptor proteins in mammals (Buck, 2004), whereas the functioning of the organ of vision, for example, requires only several types of receptor cells. (4) Unlike the majority of other species of mammals, humans use the sense of smell in their life less actively, which hampers the use of their own experience in planning experiments. (5) Observations of the behavior of animals in nature rarely make it possible to postulate that we are dealing with the olfactory signals. It is 50 years ago when Del D. Thiessen emphasized that the knowledge of the ecology of a species and its behavior, including the social structure and breeding systems, as well as the phylogenetic relationships of certain species should significantly enable the understanding of chemical communication, its functions, and the structure of olfactory signals and that a comparative study of related groups of animals will make it possible to determine the main directions of the evolution of olfactory signals, their sources, and role in interspecies isolation (Thiessen, 1977). Today, we continue to follow these principles using a multidisciplinary approach to solving the problems of chemical communication of mammals. The aim of this review was to analyze the main trends in the studies of chemical communication in mammals, developed mainly by Russian scientists (scientific school of Academician V.E. Sokolov) as well as to show which basic approaches were, and still are, used to solve specific objectives of chemical communication and what are the prospects for the development of this direction. The review will not consider the neurophysiological and psychophysiological aspects and reception of odorants. Thus, we will primarily touch on the issues related to the environmental and zoological problems. BIOLOGY BULLETIN
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*** The research of chemical communication of mammals has begun with the observation of marking behavior (Hediger, 1949). Urine, faeces, specific skin gland secretion marking of the boundaries of a home range is a very common phenomenon among mammals. This is shown, for example, for the musk deer (Prikhod’ko, 2003), a number of other species of ungulates (Muller-Schwarze, 2006), and many species of carnivorous mammals (Rozhnov, 2011). Numerous papers are devoted to the marking behavior of rodents (see, e.g., Sokolov and Gromov, 1998). In rodents (and not only), scent marks also facilitate orientation in their own home range. Apparently, they help animals to quickly find food storage left previously or the path to their burrow (Wynne-Edwards et al., 1992; Surov and Feoktistova, 2006). In addition to the “boundary marker” function, scent marks are hand over biologically significant information for other individuals. Of course, scent marks (with urine or vaginal secretions) are also important for attracting males by females during estrus. For several species of hamsters—Campbell (Phodopus campbelli), djungarian (P. sungorus), Roborovski (P. roborovskii), and gray hamster (Cricetulus migratorius)—we showed that, in nature, males find a receptive female at distances of up to several kilometers and gathered near her burrow (Surov, 2006), which can hardly be explained by causes other than the influence of olfactory signals. A similar pattern is observed in dogs, elephants, and apparently many other mammalian species. A natural continuation of the description of marking behavior and identification of possible functions of scent marks is to establish the nature of the active components of excreta. The strategy was to establish the essential and sufficient components of excreta that cause changes in the behavioral patterns and/or status of recipient. These works were performed using gas chromatography and gas chromatography–mass spectrometry, which allow for qualitative and quantitative analysis of the chemical composition of substances. Naturally, the secretion of specific skin glands, which have a strong odor, as well as feces, urine, and vaginal secretions of the species for which the respective forms of marking behavior were described, were studied as the first biologically significant chemical signals. The first such studies were performed on the civet (Civettictis civetta), musk deer (Moschus moschiferus), muskrat (Ondatra zibethicus), and beaver (Castor fiber)—species with a strong musky odor of glands determined by the presence of muscone or civetone (Lederer, 1949). It was assumed that, after determination of the chemical composition of excreta and substances present in high quantities in these excreta, we will automatically obtain the structure of the pheromone, which could be used, in particular, for practical purposes. Moreover, having identified the differences in
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the composition of excreta of males and females, receptive and nonreceptive individuals, etc., we will also be able to assess the pheromonal activity of excreta associated with gender or specific physiological state. However, it turned out that the composition of excreta markedly varies both qualitatively and quantitatively. Even if the released volatile substances had a certain attracting effect on the opposite sex, they did not promote a behavior similar to the behavior caused by native excreta (Doty, 2010). Several examples when authors managed to maximally approach to the isolation of active components from mammalian excreta are described below. The strong effect of the female vaginal secretion on the behavior of male Golden hamster (Mesocricetus auratus) (Murphy, 1980) has stimulated studies aimed at identifying its active components. Using the chromatogram of the vaginal secretion, the substance dimethyl disulfide was identified, whose concentration increased during proestrus and estrus. It was assumed that this substance is a Golden hamster’s pheromone. Indeed, its display to males of the same species caused an exploratory behavior, which was retained even if the concentration of this substance was significantly reduced (to 50%) (Singer et al., 1976). However, the response iniciated by dimethyl disulfide was still much weaker than by the whole vaginal secretion. When applied on a model (immobilized male), this substance did not stimulate the sexual behavior of males, unlike the native vaginal secretion (Macrides et al., 1977; O’Connell, 1978). For this reason, dimethyl disulfide was named a pheromonal sex attractant (Singer et al., 1976), but not a sex pheromone. Its lower activity can be explained by the fact that the vaginal secretion also contains other substances that may enhance the effectiveness of dimethyl disulfide as an attractant and, possibly, stimulate the sexual behavior in a complex with it. The activity of fatty acids, alcohols, and their mixtures, which are contained in the vaginal secretion, was also studied. However, they were inactive regardless of whether they were used independently or in combination with dimethyl disulfide (O’Connell, 1978). Other substances contained in the vaginal secretion—e.g., methylthiobutyrate (with allowance for the fact that its concentration also increases in estrus) and 18 more volatile substances and their mixtures with dimethyl disulfide—were also tested. Although the highest attractiveness was exhibited by the samples containing dimethyl disulfide, this index was still lower than that of the native vaginal secretion, and the application of these mixtures on immobilized males did not initiate sexual behavior (Singer et al., 1983). Thus, the approach to search for mammalian pheromones that can be briefly described as “source– chemical structure–bioassay” has a limited capacity and usually did not work in search for the essential and
sufficient components of excreta that could purport to be pheromones. All this has brought the researchers of mammalian chemical communication nearly to a standstill. Chemists in most cases could not propose effective methods for isolation, identification, and synthesis of biologically active signal substances. Biologists could not propose a bioassay to obtain an unambiguous answer about the activity of various compounds. A possible approach to search for the chemicals that could purport to be mammalian pheromones could be the removal of whole groups of chemical compounds rather than the determination of the complete composition of excreta, which would narrow down the range of candidates. For example, it was shown that the removal of acids or alkalies from the volatile phase of the urine of female Golden hamsters (by adding an alkali or acid, respectively) did not reduce its “attractiveness” to males. Therefore, these groups of chemicals can be regarded insignificant for the attractiveness of female urine to males. The addition of mercuric chloride to urine transforms the volatile sulfur-containing compounds to the nonvolatile ones. In this case, female urine became unattractive to males. Similarly, it was shown that sulfur-containing compounds are also responsible for coding information about the species-specific affiliation (Surov et al., 1998). Our search for the components of the vaginal secretion of Golden hamster females stimulating the sexual behavior of males by the same algorithm showed that the removal of sulfur-containing compounds from this secretion reduced the number of male that were responsive to the model. Next, we prepared a synthetic mixture of three substances that caused sexual behavior of males to the model. Thus, using the Golden hamster as an example, a multicomponent olfactory signal that causes sexual behavior of males was created for the first time for mammals. However, specific substances were not identified in native vaginal secretions (possibly due to insufficient sensitivity of available instruments). This mixture was named an artificial sex pheromone of female Golden hamsters (Sokolov et al., 1985). It may seem that a considerable success in extracting sex pheromones has been achieved in the works with the Indian elephant (Elaphus maximus). In the musth period, when the aggressiveness of males and the level of testosterone drastically increase, the temporal gland of males begins to actively production secretion. Females prefer to mate only with those males that produce more temporal gland secretion (Schulte and Rasmussen, 1999). One of the identified substances is the cyclic ketal frontalin (Rasmussen and Greenwood, 2003). The interest to this substance was determined by the fact that it is a component of the sex pheromone of the bark beetle. However, behavioral tests did not confirm its efficacy as a male sex pheromone, due to its small attractive effect. The greatest BIOLOGY BULLETIN
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response to this substance was shown by young males rather than females in estrus. However, the response to the native secretion was shown primarily by the females in the follicular phase of the cycle, whereas other females and males showed even an avoidance response. Apparently, the attractive and stimulating effect of the secretion was determined by the presence in it and many other secretions of both volatile and nonvolatile substances (Greenwood et al., 2005). It was found that the urine of estrous female Indian elephants contains a substance that attracts and stimulates males. It was identified as (Z)-7-dodecene-1-yl acetate and is also a component of sex attractants of over 126 species of insects. Its concentration in female urine greatly increases during the estrus phase. Indeed, males showed flehmen in response to both the substance isolated from urine and its synthetic analogue. However, the frequency of flehmen response was significantly lower than in the case of estrous female urine (Rasmussen et al., 1997). The authors do not rule out that this phenomenon, as in the case with frontalin, may be due to other (background) substances, including the nonvolatile ones. These nonvolatile substances form a sophisticated protein-pheromonal complex, which is apparently a prerequisite for the functioning of sex pheromones in other species of animals (Singer, 1991; Novotny, 2003). It was established experimentally that the odor of 5αandrost-16-en-3-one (androstenone) and some of its structural analogues increases the number of pigs exhibiting the lordosis response under pressure on the back as well as stimulate the onset and manifestation of heat. The effect of spraying these odorous in extremely small quantities is similar to the effect of presence of a boar and contact with him. The odor of these substances accelerates the onset of heat in female pigs and significantly increases the efficiency of their in artificial insemination (Zinkevich, 2003). It was found that the effect of the boar sex pheromone on females is not species-specific, similarly to the effect of its structural analogue, male sex hormone testosterone. The boar sex pheromone also affects the sexual cycle and reproduction of cows. Therefore, sex pheromones of male mammals apparently cannot be used as a diagnostic species trait only on the basis of the physiological responses of females (Sokolov et al., 1995). The avoidance response induced by the presentation of a predator’s odor can also be considered in the context of chemical communication (Ferrero et al., 2011). It was found that the structural pyrazine analogues contained in wolf urine are active volatile components that cause the avoidance response and overall suppressed behavior in house mice (Osada et al., 2013). The chemical composition of volatile substances of the urine of ferrets kept to different diets is quantitatively different. It was shown that Campbell hamsters distinguish by odor the ferrets fed on hamsters and the ferrets fed on mice. Thus, rodents (prey) by the odor of urine volatile components distinguish the predators that feed BIOLOGY BULLETIN
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on the representatives of their own species from the predators kept to a different diet, even if they did not encounter this species in their life (Apfelbach et al., 2015). An important aspect of the study of chemical communication is the elucidation of the chemoreception mechanisms as well as the establishment of pathways and means of transmission of olfactory information to the brain. However, the ecological and zoological focus of this review does not allow going into this topic. For this reason, we will immediately proceed to the processing of information received by a recipient individual and to the approaches that are used by researchers to determine the ability of an individual to extract useful information from the olfactory signals. It should be borne in mind that an important factor in the recognition of the gender or the physiological state of individuals as well as in an adequate response to a specified signal is the season when this occurs. For example, it is known that, for male mammals, seasonal differences in the attractiveness of odors and in responses to them are regulated by testosterone or its metabolites (Powers et al., 1985; Ferkin et al., 1994). On the other hand, the hormonal response of an organism to a presented stimulus can be serve as an index of its biological significance. The period of sensitivity to the odors of sex partners began several months before the start of breeding. The hormonal response of males, for example, could be more pronounced in spring, whereas the response to the mid-ventral gland secretion could be more pronounced in summer. Interestingly, a similar pattern of changes in the hormonal responses of males to female olfactory signals in different seasons was observed in the species belonging to different genera: Phodopus roborovskii (Feoktistova, 2008; Feoktistova and Naidenko, 2006), Allocricetulus eversmanni (Kropotkina et al., 2016), and Cricetulus barabensis griseus (Potashnikova and Feoktistova, 2014). The experimental approaches that allow identification of algorithms for the recognition of olfactory signals are scanty. We have already cited the examples of assessing the effectiveness of recognition of olfactory signals from individuals of the opposite sex of their own species, stimulation of sex or physiological responses to olfactory signals, etc. However, many issues remained unstudied. For example, researchers usually determine the ability of recipients to recognize certain parameters in conspecifics or distinguish representatives of conspecific and non-conspecific females (e.g., male–female, estrous female–anestrous female, conspecific male– non-conspecific male, etc.) by olfactory signals. The ability of animals to distinguish sign of sex or physiological state in strange species is of special value for researchers, because it allows revealing the general patterns of functioning of the communication system. In our studies, human subjects distinguished the sex of the majority exibited species of mammals by the odor of urine. Rats and dogs after learning to distinguish sex in certain species were able to attitude
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towards other ones. Male Golden hamsters without preliminary learning distinguished the odors of dogs— estrous and anestrous females as well as males (Surov et al., 2001). Thus, mammals can distinguish a certain common component in a source of olfactory signals, which, in our case, is responsible for sex and physiological state. This may indirectly confirm the hypothesis about similar components in the chemical code of sex and the physiological state in different species of mammals and the ability of animals to identify them not only in their own but also in other, even unrelated species of mammals. This can be explained by the commonness of the neuroendocrine regulation of the reproduction in different species of mammals and related differences in the metabolism of males and females, which affects the release of volatile substances. The presence of universal components in the chemical code of different mammalian species raises the question of how the “correct” sexual preferences are formed and which factors affect the perception of potential sexual partners. Early social and subsequent sexual experience may influence the olfactory preferences of adults. However, the majority of studies on this subject were performed on either normally grown animals or cross-fostering animals but without allowance for the influence of sexual experience. We have shown that Golden hamsters that were reared by rats in adulthood spend more time near the source of odor of a rat (of opposite sex) in contrast to conspecific individuals that were reared by female Golden hamsters. However, after the acquisition of sexual experience, the preference of the opposite sex of their own species was restored (Surov et al., 2004). From the standpoint of microevolutions, the attractiveness of the opposite sex of a strange species seems a useless, if not harmful, attribute (in the case where the risk of hybridization increases). However, the presence of attractive properties of excreta of individuals of the opposite sex is usually not a sufficient condition for a successful interspecific mating in mammals. During ontogeny, young animals obviously longer interact with parents and siblings and acquire first social and then sexual experiences through play and direct contacts. Formation of an adequate sexual response to the olfactory signals of individuals of the opposite sex depends not only on their own sexdependent component but also on other olfactory characteristics, such as species and individual, which together constitute an “olfactory image” of an individual and function together with the signals of other modalities (recall the concept of the biological signal field by N.P. Naumov, see above). Thus, the most important functions, such as the mate choice or an aggressive response to a stranger, in mammals cannot depend solely on chemical signals. Even in those few cases when a sexual response (for example, the effect of vaginal secretion on male Golden hamsters) or an aggressive response caused by scented model are
observed, signals of other modalities must always be present. That is, the more fully is represented the donor, the more likely is a specific behavioral response of the recipient to the chemical signal. Thus, for an adequate perception of information about another individual by olfactory signals, a set of key characters need. Moreover an image of, for example, sexual partner is formed consistently. If the basic properties (for example, the perception of sex or physiological characteristics) can be encoded genetically, the information on the species may be formed in the early ontogeny in contacts with parents and siblings (Surov, 2006). It is clear that the formation of pheromones themselves takes place under the influence of selection—more “odorous” individuals or individual with more sensitive receptors will have an advantage. Specific substances that are responsible for attracting sexual partners may also appear. Such olfactory signals will have certain group traits combining representatives of the same species, sex, or physiological state. In the case of individual odor, the issue is different—since an individual odor must be unique, the selection factor is absent as such. How the mechanism of recognition of an individual can work in this case and whether an individual odor can also be regarded a pheromone? Each individual continuously releases into the environment many hundreds of thousands of various volatile substances in very small amounts. The olfactory image of an individual may be a set of chemical components, many of which are common to all individuals but their concentrations are different or be specific to an individual. Possibly, both variants exist in parallel. Individual odor, apparently, is an integrated image including a large set of components that vary over time and depend on the state of the individual and the environment. At the same time, a unique pattern (bouquet), which allows identification of individual, is always retained. To understand the individual recognition mechanism, the most promising method is to identify a specific individual odor in a mixture with other individual odors. Dogs are able to distinguish a particular individual odor with a 100% result in a mixture consisting of 2–11 individual odors and do it reliably in more complex mixtures consisting of odors of 15 and 20 individuals. However, as the number of components in a mixture increases, the ability of dogs to distinguish a particular individual odor in it significantly decreases (Krutova and Zinkevich, 2003). We do not know what is the essential and sufficient number of components to recognize an individual by odor. This cannot be one or several substances, because in this case the number would be equal to the number of individuals. Apparently, an individual odor is an integrated image that includes a large set of components that vary over time and depend on the state of the individual and the environment. The unique patBIOLOGY BULLETIN
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tern (bouquet) that allows identification of the individual is always retained. Mammals are at the top of the pyramid of evolution of the animal world, and their senses are adapted to living in a wide range of both abiotic and biotic factors, including the social ones. The signals coming from the environment, including those from other individuals, are processed simultaneously by several sensor systems. Situations when a signal of only one modality is sufficient to stimulate a certain behavioral pattern occur quite rarely. The evolution of signaling in animals towards the generation of discrete symbol signals is not biologically justified. An animal that receives external signals each time has to decide which of them is the most important at the given moment and to respond in a certain way (Panov, 1978). According to Wilson, the prospects of development of biocommunication studies are in the synthesis of this scientific field with population genetics, population ecology, and analysis of species social systems, because only such a broad evolutionary-biological approach will allow understanding biocommunication processes and their transformations in the course of evolution (Wilson, 1975). Obviously, this directly applies to the chemical communication, which is one of the most important branches of zoology and chemical ecology. Approaches to investigation of the chemical communication in mammals include not only the elucidation of the nature of the necessary and sufficient complex of chemical signals and the study of its efficacy in various conditions but also the assessment of a significant scatter of data associated with the peculiarities of the social organization of the species, reproductive strategies, seasonal dynamics of physiological processes, as well as individual or group experience of animals. Therefore, it is extremely important to use a multidisciplinary approach combining the efforts of researchers of various profiles. As we can see, the majority of studies of the chemical communication in mammals is based on identifying the specific sources of olfactory signals and the response of animals to them. However, the information coding principles in general, the relationship between the sex, species, and physiological state signals, as well as the formation of responses of animals to them in ontogeny usually are not considered. Apparently, along with the unique elements of olfactory signals, there are universal ones encoding the basic characteristics of an animal (sex and physiological state). The idea of the universality of sex signals, for example, significantly contributes to the fundamental knowledge about the nature of sex pheromones. Unlike many foreign studies, the purpose of which was to determine the thresholds of perception or to reveal the attractiveness of olfactory signals from individuals of their own species, we believe it important to establish the ability of recipients to abstract perception of signals and isolation of single “semantic units” from them. BIOLOGY BULLETIN
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Translated by M. Batrukova