Hormones and Behavior 68 (2015) 1–2
Contents lists available at ScienceDirect
Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh
Editorial
Introduction to the special issue on chemosignals and reproduction
Communication is a critical process for reproduction as it brings animals together for mating, evaluates mating partners, supports adaptive parental care and defines defended areas and resources. For most animals and many vertebrates, the communicative process underlying reproductive success is mediated by social chemosignals or “pheromones”: chemicals that are released and/or deposited in the environment by one animal that influence the social behavior and physiology of another conspecific (likely to their mutual benefit) (Doty, 2010; Petrulis, 2013; Wyatt, 2010). Ever since the coining of the term ‘pheromone’ by Karlson and Luscher (1959), research into vertebrate chemical communication has steadily increased, both in the quantity and diversity of organisms studied. However, it is clear that with the ascendance of molecular biology, research in vertebrate chemical communication has increasingly focused on fewer species, particularly the mouse, but with greater detail. Consequently, my goal for this special issue was for it to explore both the diversity and similarity in chemical communication systems across tetrapods, including less-studied groups, (such as birds) and potentially identify productive avenues for future comparative research. In addition, the review papers in this special issue offer a broader coverage of social behaviors that are critical for reproduction (e.g. maternal and territorial behavior), rather than focusing only on copulatory behavior. Several contributions deal with the role of chemosensory cues in reproduction of non-mammalian species. First, Woodley reviews the existing literature on the role of chemosignals in reproduction of several groups of amphibians and finds that, much like in mammals, all aspects of chemical communication, from production to reaction, are regulated by hormonal mechanisms. Much of this review focuses on salamanders and newts for whom most data is available but the author also points to tantalizing suggestions that frogs and toads, a chronically understudied group with respect to chemosignaling, may also use odors to regulate their reproduction. In the second contribution, Martin and Lopez describe condition-dependent features of intrasexual (male–male competition) chemical communication in lizards, a reptile group whose chemical signaling has been examined in less detail. Specifically, the authors highlight the interactions of hormones, diet and immune system in the construction of evolutionarily honest chemosignals. Lastly, it is not a secret that the broader field has often ignored the possibility and extent of chemical communication in birds. The review by Caro, Balthazart and Bonadonna deftly lay out the reasons for this oversight, as well as making a case for a closer re-examination of the role that odors play in avian reproduction. Even if social odors may not be the dominant sensory modality for avian communication, chemosignals could still play an important role in reproduction, within the broader context of nest finding, construction and foraging.
http://dx.doi.org/10.1016/j.yhbeh.2014.12.002 0018-506X/© 2014 Elsevier Inc. All rights reserved.
Much of the work on vertebrate chemical communication has focused on mammals and this is reflected in the preponderance of reviews on how social chemosignals regulate various aspects of mammalian reproduction. Ferkin reviews his extensive body of work on meadow voles that show how a number of critical factors such as age, diet, hormone levels and body condition all influence the attractiveness of scent marks. The author emphasizes the complexity of odor-guided communication by illustrating how responsiveness to social odors is remarkably contextdependent and flexible. Examples of this include the remarkable finding of numerical competency in voles when confronted with multiple scent marks as well as the ability of voles to form complex multi-dimensional memories (“what, where, when”) using scent mark information. Processing of tetrapod social odors is often thought, incorrectly, to be the exclusive domain of the vomeronasal system. This position is often held despite decades of work showing that both the vomeronasal and main olfactory systems are important for reproduction. In their review article, Baum and Cherry articulate the critical importance of the main olfactory system for reproduction by reviewing anatomical, physiological and behavioral evidence that volatile chemosignals, mediated through the main olfactory system, drive key behavioral and hormonal aspects of successful reproduction in multiple mammalian species. They also discuss important interactions between these two chemosensory systems and how understanding this complexity may be a more accurate and productive position than previous binary conceptualizations. Martin-Sanchez et al., contribute both original research as well as a review of odor involvement in female mouse maternal and copulatory behavior, including a discussion about the male mouse urinary protein Darcin, one of the few molecules that can be considered a true mammalian pheromone. The authors identify qualitative changes in female mouse behavior (attraction to aggression) in response to Darcin as a consequence of changes in reproductive state (sexual receptivity to post-parturient). This is a particularly clear example of how receiver physiology qualitatively alters the valence/meaning of an unchanging social (odor) signal. Corona and Levy provide an excellent and updated review of the literature on how social odors impact maternal behavior in both precocial and altricial species, with an emphasis on selective maternal bonding in ungulates and humans. The authors point out that there is a surprising diversity in the role of chemosensory cues; for example, maternal behavior in rats is inhibited by pup odors whereas these odors are needed for offspring recognition in sheep. The physiological and neural mechanisms underlying odor-guided maternal behavior are discussed extensively and it is evident that hormones play a key role in altering reactions to offspring odors.
2
Editorial
Griffiths and Brennan review the literature on the role of social odor learning within a reproductive context as well as the neural mechanisms that underlie this behavioral/physiological plasticity. Their analysis agrees well with those of other contributors that emphasize the interactive nature of vomeronasal and main olfactory system contributions to social behavior and physiology. The authors also make a larger point, echoed in other contributions, that chemical communication in mammals is very flexible and highly dependent on social context and prior history. As indicated by the contribution from Griffiths and Brennan, the phenomenon whereby odors from novel males, but not from mates, can induce pregnancy failure in mice (Bruce effect) has generally been interpreted as an example of odor learning. That is, the female learns the odor of the stud male such that his odor no longer terminates pregnancy. Despite the dominance of this idea, other mechanisms may also be involved that compliment or modulate such a memory mechanism. DeCatanzaro presents the provocative hypothesis, along with supporting data, that the Bruce effect (and possibly other physiological ‘priming’ effects of social odors) may be due to female absorption of exogenous estrogens from male urine during close chemoinvestigation. Drea provides a comprehensive and comparative review of chemical communication among non-human (and human) primates. The data presented is very clear as to the importance of chemical communication in strepsirhines (e.g. lemurs, pottos, lorises) and New-World monkeys: species in these groups have steroid-dependent odor production, scent-marking and investigative behaviors as well as greater elaboration of chemosensory structures. In contrast, for other primates (including apes) the evidence for a robust chemical communication system is more suggestive than definitive. Nevertheless, the author provides compelling evidence that these primates (including humans) have greater chemosensory sensitivity and may use chemosignaling more than previously suspected.
The last contribution to this special issue is by Lubke and Pause and provides an analysis of human chemical communication within a broad reproductive context, including possible sexual attractants, maternal– infant interactions and stress-related chemosignals. The issue of human ‘pheromones’ is a controversial topic and the authors successfully balance competing perspectives. However, it is fair to say that, on balance, social odors play a much more subtle and much less critical role in human reproduction when compared to other mammals. I would like to dedicate this special issue to my friend, colleague and mentor Dr. Robert Johnston, a true pioneer in the field of vertebrate chemical communication and a strong proponent of studying and understanding the nuance, flexibility and complexity of mammalian chemical communication. References Doty, R., 2010. The great pheromone myth: mammalian pheromones, audiomones, visuomones and snarks. John Hopkins University Press, Baltimore. Karlson, P., Luscher, M., 1959. Pheromones': a new term for a class of biologically active substances. Nature 183, 55–56. Petrulis, A., 2013. Chemosignals, hormones and mammalian reproduction. Horm. Behav. 63, 723–741. 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. 196, 685–700.
Aras Petrulis Georgia State University, Neuroscience Institute, P.O. Box 5030, Atlanta, GA 30302-5030, USA E-mail address: [email protected].
Contents lists available at ScienceDirect
Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh
Editorial
Introduction to the special issue on chemosignals and reproduction
Communication is a critical process for reproduction as it brings animals together for mating, evaluates mating partners, supports adaptive parental care and defines defended areas and resources. For most animals and many vertebrates, the communicative process underlying reproductive success is mediated by social chemosignals or “pheromones”: chemicals that are released and/or deposited in the environment by one animal that influence the social behavior and physiology of another conspecific (likely to their mutual benefit) (Doty, 2010; Petrulis, 2013; Wyatt, 2010). Ever since the coining of the term ‘pheromone’ by Karlson and Luscher (1959), research into vertebrate chemical communication has steadily increased, both in the quantity and diversity of organisms studied. However, it is clear that with the ascendance of molecular biology, research in vertebrate chemical communication has increasingly focused on fewer species, particularly the mouse, but with greater detail. Consequently, my goal for this special issue was for it to explore both the diversity and similarity in chemical communication systems across tetrapods, including less-studied groups, (such as birds) and potentially identify productive avenues for future comparative research. In addition, the review papers in this special issue offer a broader coverage of social behaviors that are critical for reproduction (e.g. maternal and territorial behavior), rather than focusing only on copulatory behavior. Several contributions deal with the role of chemosensory cues in reproduction of non-mammalian species. First, Woodley reviews the existing literature on the role of chemosignals in reproduction of several groups of amphibians and finds that, much like in mammals, all aspects of chemical communication, from production to reaction, are regulated by hormonal mechanisms. Much of this review focuses on salamanders and newts for whom most data is available but the author also points to tantalizing suggestions that frogs and toads, a chronically understudied group with respect to chemosignaling, may also use odors to regulate their reproduction. In the second contribution, Martin and Lopez describe condition-dependent features of intrasexual (male–male competition) chemical communication in lizards, a reptile group whose chemical signaling has been examined in less detail. Specifically, the authors highlight the interactions of hormones, diet and immune system in the construction of evolutionarily honest chemosignals. Lastly, it is not a secret that the broader field has often ignored the possibility and extent of chemical communication in birds. The review by Caro, Balthazart and Bonadonna deftly lay out the reasons for this oversight, as well as making a case for a closer re-examination of the role that odors play in avian reproduction. Even if social odors may not be the dominant sensory modality for avian communication, chemosignals could still play an important role in reproduction, within the broader context of nest finding, construction and foraging.
http://dx.doi.org/10.1016/j.yhbeh.2014.12.002 0018-506X/© 2014 Elsevier Inc. All rights reserved.
Much of the work on vertebrate chemical communication has focused on mammals and this is reflected in the preponderance of reviews on how social chemosignals regulate various aspects of mammalian reproduction. Ferkin reviews his extensive body of work on meadow voles that show how a number of critical factors such as age, diet, hormone levels and body condition all influence the attractiveness of scent marks. The author emphasizes the complexity of odor-guided communication by illustrating how responsiveness to social odors is remarkably contextdependent and flexible. Examples of this include the remarkable finding of numerical competency in voles when confronted with multiple scent marks as well as the ability of voles to form complex multi-dimensional memories (“what, where, when”) using scent mark information. Processing of tetrapod social odors is often thought, incorrectly, to be the exclusive domain of the vomeronasal system. This position is often held despite decades of work showing that both the vomeronasal and main olfactory systems are important for reproduction. In their review article, Baum and Cherry articulate the critical importance of the main olfactory system for reproduction by reviewing anatomical, physiological and behavioral evidence that volatile chemosignals, mediated through the main olfactory system, drive key behavioral and hormonal aspects of successful reproduction in multiple mammalian species. They also discuss important interactions between these two chemosensory systems and how understanding this complexity may be a more accurate and productive position than previous binary conceptualizations. Martin-Sanchez et al., contribute both original research as well as a review of odor involvement in female mouse maternal and copulatory behavior, including a discussion about the male mouse urinary protein Darcin, one of the few molecules that can be considered a true mammalian pheromone. The authors identify qualitative changes in female mouse behavior (attraction to aggression) in response to Darcin as a consequence of changes in reproductive state (sexual receptivity to post-parturient). This is a particularly clear example of how receiver physiology qualitatively alters the valence/meaning of an unchanging social (odor) signal. Corona and Levy provide an excellent and updated review of the literature on how social odors impact maternal behavior in both precocial and altricial species, with an emphasis on selective maternal bonding in ungulates and humans. The authors point out that there is a surprising diversity in the role of chemosensory cues; for example, maternal behavior in rats is inhibited by pup odors whereas these odors are needed for offspring recognition in sheep. The physiological and neural mechanisms underlying odor-guided maternal behavior are discussed extensively and it is evident that hormones play a key role in altering reactions to offspring odors.
2
Editorial
Griffiths and Brennan review the literature on the role of social odor learning within a reproductive context as well as the neural mechanisms that underlie this behavioral/physiological plasticity. Their analysis agrees well with those of other contributors that emphasize the interactive nature of vomeronasal and main olfactory system contributions to social behavior and physiology. The authors also make a larger point, echoed in other contributions, that chemical communication in mammals is very flexible and highly dependent on social context and prior history. As indicated by the contribution from Griffiths and Brennan, the phenomenon whereby odors from novel males, but not from mates, can induce pregnancy failure in mice (Bruce effect) has generally been interpreted as an example of odor learning. That is, the female learns the odor of the stud male such that his odor no longer terminates pregnancy. Despite the dominance of this idea, other mechanisms may also be involved that compliment or modulate such a memory mechanism. DeCatanzaro presents the provocative hypothesis, along with supporting data, that the Bruce effect (and possibly other physiological ‘priming’ effects of social odors) may be due to female absorption of exogenous estrogens from male urine during close chemoinvestigation. Drea provides a comprehensive and comparative review of chemical communication among non-human (and human) primates. The data presented is very clear as to the importance of chemical communication in strepsirhines (e.g. lemurs, pottos, lorises) and New-World monkeys: species in these groups have steroid-dependent odor production, scent-marking and investigative behaviors as well as greater elaboration of chemosensory structures. In contrast, for other primates (including apes) the evidence for a robust chemical communication system is more suggestive than definitive. Nevertheless, the author provides compelling evidence that these primates (including humans) have greater chemosensory sensitivity and may use chemosignaling more than previously suspected.
The last contribution to this special issue is by Lubke and Pause and provides an analysis of human chemical communication within a broad reproductive context, including possible sexual attractants, maternal– infant interactions and stress-related chemosignals. The issue of human ‘pheromones’ is a controversial topic and the authors successfully balance competing perspectives. However, it is fair to say that, on balance, social odors play a much more subtle and much less critical role in human reproduction when compared to other mammals. I would like to dedicate this special issue to my friend, colleague and mentor Dr. Robert Johnston, a true pioneer in the field of vertebrate chemical communication and a strong proponent of studying and understanding the nuance, flexibility and complexity of mammalian chemical communication. References Doty, R., 2010. The great pheromone myth: mammalian pheromones, audiomones, visuomones and snarks. John Hopkins University Press, Baltimore. Karlson, P., Luscher, M., 1959. Pheromones': a new term for a class of biologically active substances. Nature 183, 55–56. Petrulis, A., 2013. Chemosignals, hormones and mammalian reproduction. Horm. Behav. 63, 723–741. 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. 196, 685–700.
Aras Petrulis Georgia State University, Neuroscience Institute, P.O. Box 5030, Atlanta, GA 30302-5030, USA E-mail address: [email protected].
