Pheromones
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Former Editors
ROBERT S. HARRIS KENNETH V. THIMANN
Newton, Massachusetts University of California
Santa Cruz, California
JOHN A. LORRAINE
IRA G. WOOL
University of Edinburgh
Edinburgh, Scotland University of Chicago
Chicago, Illinois
PAUL L. MUNSON
EGON DICZFALUSY
University of North Carolina
Chapel Hill, North Carolina Karolinska Sjukhuset
Stockholm, Sweden
JOHN GLOVER
ROBERT OLSEN
University of Liverpool
Liverpool, England School of Medicine
State University of New York
GERALD D. AURBACH at Stony Brook
Stony Brook, New York
Metabolic Diseases Branch
National Institute of
DONALD B. MCCORMICK
Diabetes and Digestive and
Kidney Diseases Department of Biochemistry
National Institutes of Health Emory University School of
Bethesda, Maryland Medicine, Atlanta, Georgia
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CONTENTS
Contributors xv
Preface xxi
1. Functional Neuronal Processing of Human Body Odors 1
Johan N. Lundström and Mats J. Olsson
I. The Microsmatic Fallacy 2
II. Human Body Odor Perception and Production 3
III. Central Processing of Body Odors 4
IV. Neuronal Processing of the Smell of Fear 7
V. Are Body Odors Processed by the Main Olfactory System? 12
VI. Kin Recognition via Body Odors 15
VII. The Stimulus Delivery Problem 16
VIII. Conclusion 17
Acknowledgments 18
References 18
2. Female Perception of Male Body Odor 25
Mark J. T. Sergeant
I. Olfaction in Humans 26
II. Sex Differences in Sensitivity to Body Odor 29
III. The Physiological and Behavioral Impact of Male Odor on Females 32
IV. The Effects of Odor on Mate Choice 36
V. Conclusions 39
References 40
3. Current Issues in the Study of Androstenes in Human
Chemosignaling 47
Jan Havlicek, Alice K. Murray, Tamsin K. Saxton, and S. Craig Roberts
I. Introduction 48
II. Biochemistry of Androstenes 49
III. Psychophysical Research Using Androstenes 52
IV. Psychological Effects 58
V. Discussion 68
Acknowledgments 74
References 75
vii
viii Contents
4. Mammary Odor Cues and Pheromones: Mammalian
Infant-Directed Communication about Maternal State,
Mammae, and Milk 83
Benoist Schaal
I. Introduction: Sensory Guidance to the Milk Resource
for Inexperienced, Fragile Newborns 84
II. Evolution and General Functions of Mammary Odor Cues 85
III. What Is in a Scent? Informational Intricacy in Mammary Odor 87
IV. Pan-Mammalian Distribution of Mammary Odor Cues and Signals 91
V. Regulation of Mammary Odor Cues and Pheromones 116
VI. Conclusions and Prospects 119
Acknowledgments 122
References 122
5. Exposure to Female Pheromones During Pregnancy Causes
Postpartum Anxiety in Mice 137
Caroline M. Larsen and David R. Grattan
I. Materials and Methods 139
II. Results 141
III. Discussion 146
References 148
6. Major Urinary Protein Regulation of Chemical Communication
and Nutrient Metabolism 151
Yingjiang Zhou and Liangyou Rui
I. Introduction 152
II. MUP Structure and Polymorphism 152
III. MUP Regulation of Chemical Communication 154
IV. MUP Regulation of Nutrient Metabolism 156
V. Conclusions and Future Directions 159
Acknowledgments 160
References 160
7. Chemosensory Function of the Amygdala 165
Nicolás Gutiérrez-Castellanos, Alino Martı́nez-Marcos,
Fernando Martı́nez-Garcı́a, and Enrique Lanuza
I. Introduction 168
II. Compartmentalization of the Chemosensory Amygdala 169
III. Functional Anatomy of the Chemosensory Amygdala 180
IV. Evolutionary Relevance of the Chemosensory Amygdala 186
V. Conclusions and Future Directions 189
Contents ix
Acknowledgments 189
References 189
8. TRPC Channels in Pheromone Sensing 197
Kirill Kiselyov, Damian B. van Rossum, and Randen L. Patterson
I. Pheromone Sensing Circuits 198
II. TRPC2 and Pheromone Sensing 199
III. TRPC Activation Mechanisms 200
IV. Perspectives: The ‘‘DAG Effect’’ and Beyond 207
Acknowledgments 209
References 210
9. Alarm Pheromones—Chemical Signaling in Response
to Danger 215
François J. Verheggen, Eric Haubruge, and Mark C. Mescher
I. Introduction 216
II. Alarm Pheromones in Insects 217
III. Alarm Pheromones in Marine Invertebrates 227
IV. Alarm Pheromones in Fish 228
V. Alarm Pheromones in Mammals 229
VI. Alarm Signals in Plants 230
VII. Conclusion: Potential Applications of Alarm Pheromones 231
References 232
10. Odorant-Binding Proteins in Insects 241
Jing-Jiang Zhou
I. Introduction 241
II. Diversity of Odorant-Binding Proteins 243
III. Pheromone and Ligand Binding 250
IV. Structure Aspects 259
V. Function of OBPs 262
VI. Conclusion 264
References 265
11. Drosophila CheB proteins Involved in Gustatory Detection
of Pheromones Are Related to a Human Neurodegeneration
Factor 273
Claudio W. Pikielny
I. Introduction 274
II. Drosophila CheBs Are Expressed in a Variety of Sex-Specific
Subsets of Taste Hairs that May Be Specialized in Pheromone
Detection 275
x Contents
III. CheB42a Is Required for Normal Response to Female-Specific
Pheromones 277
IV. CheBs Belong to the ML Superfamily of Lipid-Binding Proteins
and Share Functionally Important Sequences with GM2-Activator
Protein, an Essential Protein of Human Neurons 279
V. CheBs Likely Function as Gustatory-Specific Pheromone-Binding
Proteins 281
VI. Models for the Function of CheBs in Gustatory Detection
of Pheromones 283
VII. Conclusions and Future Directions 285
Acknowledgments 285
References 285
12. Volatile Signals During Pregnancy 289
Stefano Vaglio
I. Introduction 290
II. Mother Recognition 291
III. Mother–Infant Interactions 295
IV. Chemical Profile of Volatile Compounds During Pregnancy 297
V. Conclusions and Future Directions 298
Acknowledgments 301
References 301
13. Olfactory Sensitivity: Functioning in Schizophrenia and
Implications for Understanding the Nature and
Progression of Psychosis 305
Warrick J. Brewer and Christos Pantelis
I. Introduction: Overview 306
II. Structural Organisation of Olfactory Function 307
III. Olfactory Identification Deficits in Schizophrenia 309
IV. Olfactory Sensitivity Through Development 310
V. Summary and Future Directions 323
Acknowledgments 324
References 324
14. Olfactory Systems in Mate Recognition and Sexual Behavior 331
Matthieu Keller, Delphine Pillon, and Julie Bakker
I. Introduction 332
II. A Short Introduction to the Organization of the Accessory and
Main Olfactory Subsystems 333
III. Both MOS and AOS Are Functionally Involved in Pheromonal
Processing 336
Contents xi
IV. Involvement of Both Olfactory Systems in the Control of Mate
Discrimination and Sexual Behavior 340
V. General Conclusions 344
Acknowledgments 345
References 345
15. Communication by Olfactory Signals in Rabbits: Its Role
in Reproduction 351
Angel I. Melo and Gabriela González-Mariscal
I. Introduction 352
II. Communication by Chemical Signals 352
III. Other Sources of Chemical Signals 363
IV. Conclusions and Future Directions 364
Acknowledgments 367
References 367
16. Chemical Communication and Reproduction in the
Gray Short-Tailed Opossum (Monodelphis Domestica) 373
John D. Harder and Leslie M. Jackson
I. Chemical Communication and Mammalian Reproduction 374
II. Reproductive Cycles and Seasonal Breeding in Female Mammals 375
III. The Gray Short-Tailed Opossum: A Model for Pheromonal
Control of Reproduction 377
IV. Olfactory Behavior; Sources and Reception of Chemical Signals 379
V. Male Estrus-Inducing Pheromone in Opossums 384
VI. Endocrinology of Reproductive Activation 386
VII. Reproductive and Behavioral Ecology of Opossums 391
VIII. Summary and Conclusions 393
Acknowledgments 394
References 394
17. Pheromones in a Superorganism: From Gene to
Social Regulation 401
C. Alaux, A. Maisonnasse, and Y. Le Conte
I. Introduction 402
II. Physiological and Behavioral Regulation 404
III. Gene Regulation 408
IV. Social Regulation 413
V. Conclusions and Future Directions 415
Acknowledgments 418
References 418
xii Contents
18. Unraveling the Pheromone Biosynthesis Activating
Neuropeptide (PBAN) Signal Transduction Cascade that
Regulates Sex Pheromone Production in Moths 425
Shogo Matsumoto, Atsushi Ohnishi, Jae Min Lee, and J. Joe Hull
I. Introduction 426
II. Physiological Background 427
III. Molecular Background: Essential Components of B. mori
Sex Pheromone Production 430
IV. Essential Components and Mechanisms of the B. mori PBAN
Signal Transduction Cascade 435
V. Model for PBAN Signaling in B. mori 439
VI. Conclusions 440
Acknowledgments 441
References 441
19. Pheromones in Social Wasps 447
Bruschini Claudia, Cervo Rita, and Turillazzi Stefano
I. Introduction 448
II. Nestmate Recognition Pheromones 451
III. Queen Pheromones and Fertility/Rank Pheromones 461
IV. Sex Pheromones 463
V. Alarm Pheromones 466
VI. Trail and Substrate Marking Pheromones 471
VII. Defense Allomones 473
VIII. Future Directions 476
Acknowledgments 477
References 477
20. New Pheromones and Insect Control Strategies 493
Gadi V. P. Reddy and Angel Guerrero
I. Introduction 494
II. Mating Disruption in Insect Control Programs 494
III. Pheromone Antagonists as Chemical Communication Inhibitors 501
IV. Use of Pheromones with Plant-Based Volatiles 504
V. Attract-and-Kill 508
VI. Push–Pull Strategies 509
VII. Conclusions and Outlook 510
Acknowledgments 510
References 511
Contents xiii
21. Pheromones and Exocrine Glands in Isoptera 521
Ana Maria Costa-Leonardo and Ives Haifig
I. Introduction 522
II. Pheromonal Communication 523
III. Principal Exocrine Glands: Source of Pheromones 524
IV. Frontal Gland 526
V. Mandibular Glands 530
VI. Salivary or Labial Glands 531
VII. Sternal Gland 534
VIII. Tergal Gland 538
IX. Termite Recognition Pheromones 540
X. Concluding Remarks 541
Acknowledgment 542
References 542
22. Aphid Pheromones 551
Sarah Y. Dewhirst, John A. Pickett, and Jim Hardie
I. Introduction 552
II. Semiochemicals 553
III. Aphid Alarm Pheromones 554
IV. Aphid Sex Pheromone 555
V. Other Aphid Pheromones 566
VI. Conclusion 567
References 567
23. Recent Advances in Methyl Eugenol and Cue-Lure
Technologies for Fruit Fly Detection, Monitoring, and
Control in Hawaii 575
Roger I. Vargas, Todd E. Shelly, Luc Leblanc, and Jaime C. Piñero
I. Introduction 576
II. Insect Pheromones and Parapheromones 577
III. Fruit Flies and Economic Importance 578
IV. Relationship Between Male Behavior and ME and C-L/RK 580
V. Technology Development and Transfer Through the
Hawaii Area-Wide Pest Management Program 583
VI. Environmental Impact of ME and C-L/RK 587
VII. Conclusions and Future Applications 589
Acknowledgments 589
References 590
xiv Contents
24. Oviposition Pheromones in Haematophagous Insects 597
T. Seenivasagan and R. Vijayaraghavan
I. Introduction 598
II. Origin of Oviposition Pheromones 599
III. Habitat Associated Kairomones 603
IV. Microbial Volatiles Eliciting Oviposition 604
V. Parapheromones Mediating Oviposition 605
VI. Predator/Prey Released Kairomones 607
VII. Oviposition Cues of Blood Feeding Bugs 608
VIII. Oviposition Cues of Veterinary Insects 610
IX. Synthesis of Oviposition Pheromones 611
X. Evaluation of Oviposition Pheromones 612
XI. Oviposition Traps and Baits for Monitoring and Control 616
XII. Concluding Remarks 619
Acknowledgements 620
References 620
Index 631
CONTRIBUTORS
C. Alaux
INRA, UMR 406 Abeilles et Environnement, Site Agroparc, Domaine
Saint-Paul, Avignon, France
Julie Bakker
Neuroendocrinologie du Comportement, GIGA-Neurosciences, University
of Liège, Belgium, and Netherlands Institute for Neuroscience, Amsterdam,
The Netherlands, and Medical Center, Vrije Universiteit, Amsterdam,
The Netherlands
Warrick J. Brewer
ORYGEN Youth Health Research Centre, Centre for Youth Mental Health,
University of Melbourne, Victoria, Australia
Bruschini Claudia
Dipartimento di Biologia Evoluzionistica, Università degli Studi di Firenze,
Firenze, Italy
Ana Maria Costa-Leonardo
Departamento de Biologia, Instituto de Biociências, Unesp—Univ Estadual
Paulista, CEP 13506–900, Rio Claro—SP, Brasil
Sarah Y. Dewhirst
Biological Chemistry Department, Rothamsted Research, Harpenden, Herts,
United Kingdom
Gabriela González-Mariscal
Centro de Investigación en Reproducción Animal, CINVESTAV-Universidad
Autónoma de Tlaxcala, Tlaxcala, Tlax., México
David R. Grattan
Centre for Neuroendocrinology and Department of Anatomy and Structural
Biology, University of Otago, Dunedin, New Zealand
Angel Guerrero
Department of Biological Chemistry and Molecular Modeling, Institute of
Advanced Chemistry of Catalonia (CSIC), Barcelona, Spain
xv
xvi Contributors
Nicolás Gutiérrez-Castellanos
Laboratori de Neurobiologia Funcional i Comparada, Departament de Biologia
Cellular i Parasitologia, Facultat de Ciències Biològiques, Universitat de València,
Dr. Moliner, 50, Burjassot, València, Spain
Ives Haifig
Departamento de Biologia, Instituto de Biociências, Unesp—Univ Estadual
Paulista, CEP 13506–900, Rio Claro—SP, Brasil
John D. Harder
Department of Evolution, Ecology, and Organismal Biology, The Ohio State
University, Columbus, Ohio
Jim Hardie
Department of Life Sciences, Imperial College London, Silwood Park campus,
Ascot, Berkshire, United Kingdom
Eric Haubruge
Department of Functional and Evolutionary Entomology, Gembloux Agro-Bio
Tech, Liege University, Gembloux, Belgium
Jan Havlicek
Department of Anthropology, Faculty of Humanities, Charles University, Prague,
Czech Republic
J. Joe Hull
Molecular Entomology Laboratory, RIKEN Advanced Science Institute, Wako,
Saitama, Japan, and USDA-ARS Arid Land Agricultural Research Center, 21881
N Cardon Lane, Maricopa, Arizona, USA
Leslie M. Jackson
Department of Evolution, Ecology, and Organismal Biology, The Ohio State
University, Columbus, Ohio
Matthieu Keller
INRA, UMR 85 Physiologie de la Reproduction et des Comportements,
Nouzilly, France, and CNRS, UMR 6175, Nouzilly, France, and Université
François Rabelais de Tours, Tours, France
Kirill Kiselyov
Department of Biological Sciences, University of Pittsburgh, Pittsburgh,
Pennsylvania, USA
Enrique Lanuza
Laboratori de Neurobiologia Funcional i Comparada, Departament de Biologia
Cellular i Parasitologia, Facultat de Ciències Biològiques, Universitat de València,
Dr. Moliner, 50, Burjassot, València, Spain
Caroline M. Larsen
Centre for Neuroendocrinology and Department of Anatomy and Structural
Biology, University of Otago, Dunedin, New Zealand
Contributors xvii
Y. Le Conte
INRA, UMR 406 Abeilles et Environnement, Site Agroparc, Domaine
Saint-Paul, Avignon, France
Luc Leblanc
Department of Plant Environmental Protection Science, University of Hawaii,
Honolulu, Hawaii, USA
Jae Min Lee
Molecular Entomology Laboratory, RIKEN Advanced Science Institute, Wako,
Saitama, Japan
Johan N. Lundström
Monell Chemical Senses Center, Philadelphia, Pennsylvania, USA, and
Department of Psychology, University of Pennsylvania, Pennsylvania, USA, and
Section of Psychology, Department of Clinical Neuroscience, Karolinska Institute,
Stockholm, Sweden
A. Maisonnasse
INRA, UMR 406 Abeilles et Environnement, Site Agroparc, Domaine
Saint-Paul, Avignon, France
Fernando Martı́nez-Garcı́a
Laboratori de Neurobiologia Funcional i Comparada, Departament de Biologia
Funcional i Antropologia Fı́sica, Facultat de Ciències Biològiques, Universitat de
València, Dr. Moliner, 50, Burjassot, València, Spain
Alino Martı́nez-Marcos
Laboratorio de Neuroanatomı́a Humana, Departamento de Ciencias Médicas,
Facultad de Medicina, Centro Regional de Investigaciones Biomédicas,
Universidad de Castilla-La Mancha, Albacete, Spain, and Fac. Medicina Ciudad
Real (UCLM). Avda. MOledores S/N. 13071 Ciudad Real
Shogo Matsumoto
Molecular Entomology Laboratory, RIKEN Advanced Science Institute, Wako,
Saitama, Japan
Angel I. Melo
Centro de Investigación en Reproducción Animal, CINVESTAV-Universidad
Autónoma de Tlaxcala, Tlaxcala, Tlax., México
Mark C. Mescher
Department of Entomology, Center for Chemical Ecology, The Pennsylvania
State University, University Park, Pennsylvania, USA
Alice K. Murray
School of Biological Sciences, University of Liverpool, Liverpool, UK
xviii Contributors
Atsushi Ohnishi
Molecular Entomology Laboratory, RIKEN Advanced Science Institute, Wako,
Saitama, Japan
Mats J. Olsson
Section of Psychology, Department of Clinical Neuroscience, Karolinska Institute,
Stockholm, Sweden
Christos Pantelis
Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of
Melbourne, Victoria, Australia
Randen L. Patterson
Department of Biology, and Center for Computational Proteomics, The Pennsyl-
vania State University, University Park, Pennsylvania, USA
Jaime C. Piñero
Department of Plant Environmental Protection Science, University of Hawaii,
Honolulu, Hawaii, USA, and Cooperative Research and Extension, Lincoln
University of Missouri, Jefferson City, Missouri, USA
John A. Pickett
Biological Chemistry Department, Rothamsted Research, Harpenden, Herts,
United Kingdom
Claudio W. Pikielny
Department of Genetics and Neuroscience Center, Dartmouth Medical School,
Hanover, New Hampshire, USA
Delphine Pillon
INRA, UMR 85 Physiologie de la Reproduction et des Comportements,
Nouzilly, France, and CNRS, UMR 6175, Nouzilly, France, and Université
François Rabelais de Tours, Tours, France
Gadi V. P. Reddy
Western Pacific Tropical Research Center, College of Natural and Applied
Sciences, University of Guam, Mangilao, Guam, USA
Cervo Rita
Dipartimento di Biologia Evoluzionistica, Università degli Studi di Firenze,
Firenze, Italy
S. Craig Roberts
School of Biological Sciences, University of Liverpool, Liverpool, UK
Liangyou Rui
Department of Molecular & Integrative Physiology, University of Michigan
Medical School, Ann Arbor, Michigan, USA
Contributors xix
Tamsin K. Saxton
Philosophy, Psychology and Language Sciences, University of Edinburgh, Edinburgh,
UK
Benoist Schaal
Research Group in Developmental Ethology and Cognitive Psychology, Center
for Taste and Smell Science, CNRS, Dijon, France
Mark J. T. Sergeant
Division of Psychology, Nottingham Trent University, Nottingham, United
Kingdom
T. Seenivasagan
Defence Research & Development Establishment, Ministry of Defence,
Government of India, Jhansi Road, Gwalior-474 002, MP, India
Todd E. Shelly
USDA-APHIS, Waimanalo, Hawaii, USA
Turillazzi Stefano
Dipartimento di Biologia Evoluzionistica, Università degli Studi di Firenze,
Firenze, Italy, and Centro Interdipartimentale di Spettrometria di Massa
(C.I.S.M.), Università degli Studi di Firenze, Firenze, Italy
Stefano Vaglio
Laboratory of Anthropology, Department of Evolutionary Biology ‘‘Leo Pardi,’’
University of Florence, Florence, Italy
Damian B. van Rossum
Department of Biology, and Center for Computational Proteomics, The Pennsyl-
vania State University, University Park, Pennsylvania, USA
Roger I. Vargas
U.S. Pacific Basin Agricultural Research Center, USDA, ARS, Hilo, Hawaii, USA
François J. Verheggen
Department of Functional and Evolutionary Entomology, Gembloux Agro-Bio
Tech, Liege University, Gembloux, Belgium
R. Vijayaraghavan
Defence Research & Development Establishment, Ministry of Defence,
Government of India, Jhansi Road, Gwalior-474 002, MP, India
Jing-Jiang Zhou
Centre for Sustainable Pest and Disease Management, Insect Molecular Biology
Group, Biological Chemistry Division, Rothamsted Research, Harpenden, UK
Yingjiang Zhou
Department of Molecular & Integrative Physiology, University of Michigan Med-
ical School, Ann Arbor, Michigan, USA
PREFACE
Pheromones are chemical substances generated by an individual that can
affect another individual. The sensing individual may respond by some kind
of specific response varying from alarm reactions to sexual behavior and to
specific types of behavior in lower forms. The phenomenology of phero-
mones is particularly well documented for insects. Pheromone chemicals
vary considerably from specie to specie. In this volume are reviewed many
of the types of pheromones and their actions.
The volume opens with reviews of a more general nature and those
that apply to humans in some cases. The first chapter deals with ‘‘Functional
Neuronal Processing of Human Body Odors’’ by J. N. Lundstrom and
M. J. Olsson. ‘‘Female Perception of Male Body Odor’’ is contributed by
M. J. T. Sergeant. This is followed by ‘‘Current Issues in the Study of
Androstenes in Human Chemosignalling’’ by J. Havlicek, A. K. Murray,
T. K. Saxton, and S. C. Roberts. B. Schaal discusses ‘‘Mammary Odor Cues
and Pheromones: Mammalian Infant-directed Communication about Mater-
nal State, Mammae, and Milk.’’ C. M. Larsen and D. R. Grattan describe
‘‘Exposure to Female Pheromones during Pregnancy causes Postpartum
Anxiety in Mice.’’ ‘‘Major Urinary Protein Regulation of Chemical Com-
munication and Nutrient Metabolism’’ is reviewed by Y. Zhou and L. Rui.
‘‘Chemosensory Function of the Amygdala’’ is recorded by N. Gutierrez-
Castellanos, A. Martinez-Marcos, F. Martinez-Garcia, and E. Lanuza.
K. Kiselyov, D. B. van Rossum, and R. L. Patterson report on ‘‘TRPC
Channels in Pheromone Sensing.’’ ‘‘Alarm Pheromones: Chemical Signaling
in Response to Danger’’ is the topic of F. J. Verheggen, E. Haubruge, and
M. C. Mescher. Jiang-Jing Zhou describes ‘‘Odorant Binding Proteins in
Insects’’ and C. W. Pikielny writes on ‘‘Drosophila CheB Proteins Involved in
Gustatory Detection of Pheromones are Related to a Human Neurodegen-
eration Factor.’’ S. Vaglio reports on ‘‘Volatile Signals During Pregnancy’’
and ‘‘Olfactory Sensitivity: Functioning in Schizophrenia and Implications
for Understanding the Nature and Progression of Psychosis.’’ This is followed
by ‘‘Olfactory Systems in Mate Recognition and Sexual behavior’’ by
M. Keller, D. Pillon, and J. Bakker. The last two chapters in this introductory
section are those of A. I. Melo and G. Gonzalez-Mariscal on ‘‘Communica-
tion by Olfactory Signals in Rabbits: its Role in Reproduction’’ and ‘‘Chem-
ical Communication and Reproduction in the Gray Short-tailed Opossum’’
(Monodelphis domestica) by J. D. Harder and L. M. Jackson.
A major topic in the discussion of pheromones is the information about
lower forms, especially in the insect world. This is the area where a great deal
xxi