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Sex Pheromones and Their Role in Vertebrate Reproduction

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Sex Pheromones and Their Role in Vertebrate Reproduction Intraspecific chemical communication in vertebrates with special attention to sex pheromones Robert van den Hurk Pheromone Information Centre, Brugakker 5895, 3704 MX Zeist, The Netherlands Pheromone Information Centre, Zeist, The Netherlands. Correspondence address: Dr. R. van den Hurk, Brugakker 5895, 3704 MX Zeist. E-mail address: [email protected] Intraspecific chemical communication in vertebrates with special attention to sex pheromones (191 pp). NUR-code: 922. ISBN: 978-90-77713-78-5. © 2011 by R. van den Hurk. Second edition This book is an updated edition from a previous book entitled: ‘Intraspecific chemical communication in vertebrates with special attention to its role in reproduction, © 2007 by R. van den Hurk. ISBN: 978-90-393-4500-9. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording or any information storage and retrieval system, without permission in writing from the author. Printed by EZbook.nl 2 Contents Abbreviations 5 Preface 6 Abstract 7 Introduction 8 Sex pheromones in fishes 14 Gobies 14 Zebrafish 15 African catfish 21 Goldfish 26 Other fish species 30 Reproduction and nonolfactory sensory cues 35 Sex pheromones in amphibians 37 Red-bellied newt 37 Sword-tailed newt 37 Plethodontid salamanders 38 Ocoee salamander 38 Korean salamander 39 Magnificent tree frog (Litoria splendida) and mountain chicken frog (Leptodactylus fallax) 39 Other amphibian species 39 Sex pheromones in reptiles 42 Lizards 42 Turtles 43 Snakes 43 Crocodiles 45 Sex pheromones in birds 46 Sex pheromones in mammals 48 Introductory information on MHC peptides, lipocalins, MUPs and vomeronasal binding proteins 48 Marsupials 52 Rodents (mice, rats, voles, lemmings, hamsters, and beavers) and rabbits 53 Carnivores 62 Felines 62 Canines 71 Mustelids 71 Bears 74 Ungulates 74 Pigs 74 Camels and giraffes 76 Deers and antelopes 76 Cows 79 Buffaloes 82 Sheep and goates 82 Horses 84 Elephants 84 Primates 86 Humans 86 Nonhuman primates 95 3 Olfactory receptor sites, odourant and pheromonal perception, signal transduction, and conduction of evoked action potentials to and within the brain 99 Mammals 99 Olfactory chemoreceptors in the MOS 99 Signal transduction after odourant-OR binding in the MOS 101 Conduction of action potentials evoled by OR neurons from the MOS to and within the brain 102 The VNO 104 Signal transduction after pheromone-VR binding in the VNO 111 Conduction of action potentials evoled by VR neurons from the VNO to and within the brain 114 Functional relation between the MOS and the VNO 117 Human brain responses to putative pheromones 118 Olfactory chemoreceptors different from ORs and VRs 119 The septal organ and Grüneberg ganglion as possible detection sites for odourants or pheromones 121 The trigeminal nerve and odourant/pheromone perception 122 Direct stimulation of the brain by odourants/pheromones 123 Nonmammalian vertebrates 123 Fishes 124 Amphibians 126 Reptiles 128 Birds 128 Concluding remarks and future perspectives 129 Refererences 134 Epilogue 190 About the author 191 4 Abbreviations: ADIO: androstadienone, a putative male (human) modulator pheromone AOB: accessory olfactory bulb AD: 4-androsten-3, 17-dione GNG(C): Golf-cyclic nucleotid-gated (channel) DAG: diacylglycerol DAP: dog appeasing pheromone EAP: equine appeasing pheromone EOG: electro-olfactogram ESP exocrine gland-secreting peptide EST: oestratetraenol, a putative female (human) modulator pheromone EVG: electrovomeronasogram GC-MS: gas chromatography-mass spectrometry GnRH: gonadotropin-releasing hormone GtH: gonadotropic hormone HSD hydroxy-steroid dehydrogenase IP3: inositol-1,4,5-triphosphate LASP: Leptodactylus aggression-stimulating peptide LH: luteinizing hormone LHRH: luteinizing-hormone-releasing hormone MHC: major histocompatibility complex MHUSA: mother-hen uropygial secretion analogue MOB: main olfacory bulb MOS: main olfactory system MOE: epithelium of the main olfactory system MRI: magnetic resonance imaging MUP: major urinary protein NO(S): nitric oxide (synthetase) NW: new world OB: olfactory bulb OBP: odourant binding protein ORN: olfactory receptor neuron OR: olfactory receptor OW: old world PET positron emission tomography PG prostaglandin PIP2: phosphoinsositol-4,5-biphosphate PLC: phospholipase C PMF: Plethodon modulatory factor PRF: Plethodontid receptivity factor PRL: prolactin PZS: petromyzonol sulphate SAL: salivery protein SPF: sodefrin precursor-like factor TRP2: transient receptor potential type 2 UG: urogenital VEG: Von Ebner’s gland VNBP: vomeronasal binding protein VNE: vomeronasal epithelium VNO: vomeronasal organ VNS: vomeronasal system VR: vomeronasal receptor VRN: vomeronasal receptor neuron ZDA: (Z)-7-dodecen-1-yl acetate, a urinary female Asian elephant sex pheromone 17,20P: 4-pregnene-17α, 20β-diol-3-one 17,20P-S: 4-pregnene-17α, 20β-diol-3-one sulphate 17,20P-G: 4-pregnene-17α, 20β-diol-3-one glucuronide 5 Acknowledgements: The author thanks Dr. Regiane Santos and Pim van den Hurk for their contribution to the lay- out of tables and figures. Photographs in this review were obtained from Dr. Jan-Willem Resink. Preface In this review you will find a survey of pheromonal processes in Vertebrates, the source where they are formed, the chemical nature of pheromones or putative pheromones, the sites where pheromones are perceived, and the way in which they can exert their effects. I hope, in this way, to please researchers at this field and to make many students enthusiastic to start studies on pheromones. Besides, I hope to make clear that this kind of research is important or could be important for application in catching and breeding of fish, husbandry and production of farm animals, housing of companion animals, integrated management of harmful animals (like beavers which, in dense populations, may cause enormous damage to nature), reproduction of endangered animal species, and behaviour of the human. This 2011 review is an updated edition from the book entitled ‘Intraspecific chemical communication in vertebrates with special attention to its role in reproduction’ (Van den Hurk, 2007). This book was sent to many leading figures on the field of vertebrate sex pheromones of which many reacted very praiseworthy. At the internete site ‘http://scentoferos.com/ScientificEvidence.html’, the book was announced as ‘the most recent comprehensive pheromone review available’. Because of the enthousiastic reactions, I decided to make an update of this review and to correct the many typographical errors and a few interpretation mistakes that were made in the book. With the appearance of the 2011 edition, it now becomes the most recent and most comprehensive pheromone review available. After the publishing of the first edition in February 2007, world-wide attention of pheromone research was particularly directed to odourant/pheromone receptors and signal transduction within odourant/pheromone sensing cells. Therefore, in this 2011-edition of the book, the chapter dealing with olfactory receptor sites, odourant and pheromonal perception, signal transduction, and conduction of evoked action potentials to and within the brain has substantially been changed, while new information published until January 2011 has been incorporated. As a consequence, Table 15 and the original Figure 11 (the current Figure 9) had to be adapted, while Table 16 and Figure 10 were newly added. Furthermore, most tables are extended with new data on pheromones in vertebrate species. To focus more on the term (sex) pheromone and to facilitate tracing of the current book, the original book title has slightly been changed. Please, contact me ([email protected]) if you think some essential things are lacking or incorrectly presented. 6 Abstract Sex pheromones in fish can be formed by the liver, the gonads and/or accessory sex organs, excreted through the urogenital efferent duct system, the faeces, the gills or the skin, and may play a role in the development of gonads, the attraction of reproductive partners, reproductive behaviour, sperm production or ovulation induction. In teleost fish, steroid glucuronides, steroid sulphates, free steroids and prostaglandines may function as sex pheromones, while in lampreys, bile acids are used as odourants for successful spawning. In amphibians, abdominal glands and fascial glands may secrete specific peptides or proteins as sex pheromones. In reptiles, the skin, pre-cloacal glands, femoral glands and seminal fluid are possible sources of sex pheromones, while in birds it is the uropygial gland which has this function. A mixture of specific methyl ketones has been indicated as a sex pheromone in snakes, whereas specific fatty acid diesters have been proved to serve as duck pheromones. Many classes of chemical compounds have been found to play or are thought to play a role as (sex) pheromones in mammals. They are produced by the urinary system, the digestive tract and/or all kind of glands. Olfactory signs may be secreted pulsatily in a species-specific mixture of components, of which the concentration and relative proportion is appropriate reproductive information and govern sexual behaviour. Besides olfactory signs, initiation and completion of adequate reproduction behaviour is additionally controlled by other sensory cues, like taste, visual, vibrational, tactile and/or auditory stimuli. Apart from the source, the nature and the role of (sex) pheromones in vertebrates, information is given
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