Ebook Hormones and reproduction of vertebrates (Vol 4 - Birds): Part 1

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Part 1 book "Hormones and reproduction of vertebrates (Vol 4 - Birds)" includes content: Neuroendocrine control of reproduction in birds; avian testicular structure, function, and regulation; organization and functional dynamics of the avian ovary; maternal hormones in avian eggs.

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Hormones and Reproduction of Vertebrates, Volume 1dFishes Hormones and Reproduction of Vertebrates, Volume 2dAmphibians Hormones and Reproduction of Vertebrates, Volume 3dReptiles Hormones and Reproduction of Vertebrates, Volume 4dBirds Hormones and Reproduction of Vertebrates, Volume 5dMammals
Hormones and Reproduction of Vertebrates Volume 4: Birds David O. Norris Department of Integrative Physiology University of Colorado Boulder, Colorado Kristin H. Lopez Department of Integrative Physiology University of Colorado Boulder, Colorado AMSTERDAM BOSTON HEIDELBERG LONDON NEW YORK OXFORD PARIS SAN DIEGO SAN FRANCISCO SINGAPORE SYDNEY TOKYO Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA First edition 2011 Copyright Ó 2011 Elsevier Inc. All rights reserved Cover images Front cover image: Amphiprion percula, the orange clownﬁsh. Courtesy of iStockphoto: Image 6571184. Back cover image: Atlantic hagﬁsh (Myxine glutinosa) eggs. Courtesy of Stacia A. Sower, University of New Hampshire, Durham, NH, USA and Scott I. Kavanaugh, University of Colorado, Boulder, CO, USA. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: permissions@elsevier.com. Alternatively, visit the Science and Technology Books website at www.elsevierdirect.com/rights for further information. Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent veriﬁcation of diagnoses and drug dosages should be made. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress. ISBN: 978-0-12-374932-1 (Set) ISBN: 978-0-12-375009-9 (Volume 1) ISBN: 978-0-12-374931-4 (Volume 2) ISBN: 978-0-12-374930-7 (Volume 3) ISBN: 978-0-12-374929-1 (Volume 4) ISBN: 978-0-12-374928-4 (Volume 5) For information on all Academic Press publications visit our website at elsevierdirect.com Typeset by TNQ Books and Journals Pvt Ltd. www.tnq.co.in Printed and bound in United States of America 10 11 12 13 14 15 10 9 8 7 6 5 4 3 2 1
Dedication This series of ﬁve volumes on the hormones and reproduction of vertebrates is appropriately dedicated to our friend and colleague of many years, Professor Emeritus Richard Evan Jones, who inspired us to undertake this project. Dick spent his professional life as a truly comparative reproductive endocrinologist who published many papers on hormones and reproduction in ﬁshes, amphibians, reptiles, birds, and mammals. Additionally, he published a number of important books including The Ovary (Jones, 1975, Plenum Press), Hormones and Reproduction in Fishes, Amphibians, and Reptiles (Norris and Jones, 1987, Plenum Press), and a textbook, Human Reproductive Biology (Jones & Lopez, 3rd edition 2006, Academic Press). Throughout his productive career he consistently stressed the importance of an evolutionary perspective to understanding reproduction and reproductive endocrinology. His enthusiasm for these subjects inspired all with whom he interacted, especially the many graduate students he fostered, including a number of those who have Richard Evan Jones contributed to these volumes. v
Preface Hormones and Reproduction of Vertebrates Preface to the Series Every aspect of our physiology and behavior is either Chemical pollution and climate change pose serious regulated directly by hormones or modiﬁed by their challenges to the conservation and reproductive health of actions, as exempliﬁed by the essential and diverse roles of wildlife populations and humans in the twenty-ﬁrst century, hormones in reproductive processes. Central to the evolu- and these issues must be part of our modern perspective on tionary success of all vertebrates are the regulatory chem- reproduction. Consequently, we have included chapters that icals secreted by cells that control sexual determination, speciﬁcally deal with the accumulation of endocrine- sexual differentiation, sexual maturation, reproductive disrupting chemicals (EDCs) in the environment at very physiology, and reproductive behavior. To understand these low concentrations that mimic or block the critical functions processes and their evolution in vertebrates, it is necessary of our reproductive hormones. Many authors throughout the to employ an integrated approach that combines our series also have provided information connecting repro- knowledge of endocrine systems, genetics and evolution, ductive endocrinology to species conservation. and environmental factors in a comparative manner. In The series consists of ﬁve volumes, each of which deals addition to providing insight into the evolution and physi- with a major traditional grouping of vertebrates: in volume ology of vertebrates, the study of comparative vertebrate order, ﬁshes, amphibians, reptiles, birds, and mammals. reproduction has had a considerable impact on the Each volume is organized in a similar manner so that biomedical sciences and has provided a useful array of themes can be easily followed across volumes. Termi- model systems for investigations that are of fundamental nology and abbreviations have been standardized by the importance to human health. The purpose of this series on editors to reﬂect the more common usage by scientists the hormones and reproduction of vertebrates is to bring working with this diverse assembly of organisms we together our current knowledge of comparative reproduc- identify as vertebrates. Additionally, we have provided tive endocrinology in one place as a resource for scientists indices that allow readers to locate terms of interest, involved in reproductive endocrinology and for students chemicals of interest, and particular species. A glossary of who are just becoming interested in this ﬁeld. abbreviations used is provided with each chapter. In this series of ﬁve volumes, we have selected authors Finally, we must thank the many contributors to this with broad perspectives on reproductive endocrinology work for their willingness to share their expertise, for their from a dozen countries. These authors are especially timely and thoughtful submissions, and for their patience knowledgeable in their speciﬁc areas of interest and are with our interventions and requests for revisions. Their familiar with both the historical aspects of their ﬁelds and chapters cite the work of innumerable reproductive biolo- the cutting edge of today’s research. We have intentionally gists and endocrinologists whose efforts have contributed included many younger scientists in an effort to bring in to this rich and rewarding literature. And, of course, our fresh viewpoints. Topics in each volume include sex deter- special thanks go to our editor, Patricia Gonzalez of mination, neuroendocrine regulation of the hypothalamuse Academic Press, for her help with keeping us all on track pituitaryegonadal (HPG) axis, separate discussions of and overseeing the incorporation of these valuable contri- testicular and ovarian functions and control, stress and butions into the work. reproductive function, hormones and reproductive behav- iors, and comparisons of reproductive patterns. Emphasis on David O. Norris the use of model species is balanced throughout the series with comparative treatments of reproductive cycles in major Kristin H. Lopez taxa. xiii
Preface Preface to Volume 4 Birds Birds are unique among vertebrates in that they are highly This avian volume on hormones and reproduction adapted for ﬂight in terms of their anatomy, physiology, and focuses both on bird species in wild populations and on behavior. Further, they are possibly the most visible captive birds, in which reproductive physiology and vertebrate species to humans in being strongly diurnal, behavior may be studied relatively easily. We begin with often brightly colored, and extremely easy to observe in a chapter on the neuroendocrine regulation of reproduc- their natural habitats. Consequently, birds have been tion and follow with chapters on testicular and ovarian a favorite target for biologists interested in studying the functions. Following is a discussion of the maternal role relationships among hormones, natural environmental in determining the hormonal and nutrient composition of factors, and reproduction in wild vertebrates. the egg and its signiﬁcance for successful reproduction. Distributed in a wide range of habitats globally, all birds Chapters on the hormones involved in stress, courtship are characterized physiologically by endothermy, internal and mating behavior, parental behavior, and migration fertilization, and obligate oviparity. Females produce rela- and reproductive cycles represent the emphases of the tively small numbers of large yolky eggs, and embryonic study of bird reproduction over the past several development generally requires elevated temperatures, decades. Finally, the importance of endocrine disruption provided by brooding. Thus, considerable parental care is in bird populations by anthropogenic chemicals is involved in the successful reproduction of most bird species. discussed. xv
Contributors Sarah J. Alger, University of Wisconsin, Madison, WI, USA Moira McKernan George E. Bentley, University of California at Berkeley, Berkeley, Mary Ann Ottinger, University of Maryland, College Park, MD, CA, USA USA Creagh W. Breuner, University of Montana, Missoula, MT, USA Michael J. Quinn, Jr. Karen Dean Marilyn Ramenofsky, University of California, Davis, CA, USA Pierre Deviche, Arizona State University, Tempe, AZ, USA Takayoshi Ubuka, University of California at Berkeley, Berkeley, CA, USA H. Bobby Fokidis, Arizona State University, Tempe, AZ, USA Lauren V. Riters, University of Wisconsin, Madison, WI, USA Ton G.G. Groothuis, University of Groningen, Haren, The Netherlands Carol M. Vleck, Iowa State University, Ames, IA, USA Laura L. Hurley, Arizona State University, Tempe, AZ, USA David Vleck, Iowa State University, Ames, IA, USA A.L. Johnson, The Pennsylvania State University, University Park, Nikolaus von Engelhardt, University of Bielefeld, Bielefeld, PA, USA Germany xvii
Chapter 1 Neuroendocrine Control of Reproduction in Birds Takayoshi Ubuka and George E. Bentley University of California at Berkeley, Berkeley, CA, USA Passeriformes include all songbirds, and contain more than SUMMARY Reproductive physiology and behavior of birds are ultimately half of all bird species (Sibley & Monroe, 1990). controlled by the hypothalamusehypophysial system. Hypotha- Reproductive activities of birds consist of multiple lamic neurons integrate internal and external signals, controlling stages in their life history. Typically, males establish reproduction by releasing neurohormones to the adenohypophysis territories after the initiation of gonadal maturation and (anterior pituitary). Reproductive activation occurs via gonado- form pairs with females. Male and female birds mature tropin-releasing hormone (GnRH) stimulation of adenohypo- their gonads and engage in courtship, construct nests, physial gonadotropin secretion. Gonadotropins (GTHs) and copulate, and female birds ovulate and lay eggs. (luteinizing hormone (LH), follicle-stimulating hormone (FSH)) After incubating their eggs, they feed nestlings and act on the gonads to stimulate gametogenesis and sex steroid ﬂedglings. Finally, the reproductive system regresses and production. Gonadotropin-inhibiting hormone (GnIH) may inhibit the next life-history stage follows, e.g., molt (Wingﬁeld gonadotropin secretion directly or indirectly by decreasing the et al., 1999). Many passerine species that breed at high activity of GnRH neurons. Another adenohypophysial hormone that plays an important role in avian reproduction is prolactin latitudes incorporate two migratory periods between (PRL). The secretion of PRL is thought to be regulated by nonbreeding and breeding stages (Wingﬁeld & Farner, a hypothalamic neuropeptide, vasoactive intestinal peptide. 1980). Arginine vasotocin (AVT) is released from the neurohypophysis Reproductive physiology and behavior of birds are (posterior pituitary) and regulates oviposition by directly inducing governed by the hypothalamic (neuroendocrine) control uterine contraction. Several mechanisms are discussed in terms of of pituitary hormone secretion (hypothalamusepituitary how the brain perceives and translates external environmental system (HPS)). Accordingly, this chapter will start with information into internal hormonal signals to time seasonal a brief summary of the anatomy of the HPS and the reproduction. neurohormones involved in avian reproduction. Gonad- otropins (GTHs) (luteinizing hormone (LH), follicle- stimulating hormone (FSH)) are important anterior pitu- itary hormones that control avian reproduction by inducing gametogenesis (spermatogenesis, oogenesis) 1. INTRODUCTION and sex steroidogenesis (androgens, estrogens, proges- Birds (class Aves) are bipedal, homeothermic oviparous togens) in the gonad. Accordingly, investigation of how vertebrate animals. Modern birdsdcomprising nearly the hypothalamic neurohormones control GTH secretion 10 000 living speciesdare divided basally into two clades, from the pituitary is imperative to understand the Palaeognathae and Neognathae (Harshman, 2006). Palae- neuroendocrine control of reproduction. Two hypotha- ognathae includes the ratites (e.g. ostrich (Struthio cam- lamic neuropeptides, gonadotropin-releasing hormone elus), emu (Dromaius novaehollandiae), and kiwis (GnRH) and gonadotropin-inhibitory hormone (GnIH), (Apteryx)) and tinamous. Neognathae is divided into Gal- which have opposite effects on GTH secretion, will be loanserae and Neoaves. Galloanserae consist of the sister introduced. Ovulation and egg-laying (oviposition) are orders Anseriformes (e.g., ducks, geese, and swans) and highly orchestrated female reproductive actions that Galliformes (e.g., turkeys, grouse, chickens, quail, and involve various hormones. Another hypothalamic neuro- pheasants). Neoaves consist of 24 orders, including hormone, arginine vasotocin (AVT), is released directly Columbiformes (pigeons, doves) and Passeriformes. from the neurohypophysis and induces oviposition. After Hormones and Reproduction of Vertebrates, Volume 4dBirds 1 Copyright Ó 2011 Elsevier Inc. All rights reserved.
2 Hormones and Reproduction of Vertebrates oviposition, incubation of the eggs and feeding of the 2. THE HYPOTHALAMUSePITUITARY offspring are the typical next stages in avian life history. SYSTEM (HPS) These parental behaviors seem to be controlled by another anterior pituitary hormone, prolactin (PRL). Reproductive activity of birds is controlled by the HPS. Hypothalamic vasoactive intestinal peptide (VIP) is Hypothalamic neurons somehow integrate external (light, thought to regulate PRL secretion from the anterior temperature, sound, etc.) and internal (water, nutrition, pituitary. Many birds reproduce seasonally. How do birds hormones, etc.) information, and regulate the reproductive perceive and translate external environmental informa- physiology and behavior of the bird by releasing neuro- tion into internal hormonal signals to time reproduction? hormones to the pituitary. Figure 1.1 shows the general- If reproductive physiology and behavior of birds are ized anatomical structure of the hypothalamus and ultimately controlled by the HPS, how does this system pituitary in the avian brain (Stokes, Leonard, & Notte- control seasonal reproductive activities of birds? Does bohm, 1974; Foster, Plowman, Goldsmith, & Follett, the hypothalamus detect the external environmental 1987; Matsumoto & Ishii, 1992). Table 1.1 summarizes signals itself, or are they detected by other organs and the the molecular structures and the known functions of the information transduced to the hypothalamic neuronal identiﬁed key neurohormones that control reproduction in system to control pituitary hormone secretion? These birds. The neuroendocrine system controlling reproduc- interesting topics will be discussed in Section 3. Finally, tion of birds is summarized in Figure 1.2. Various we will investigate the lines of research that will be neurohormones that seem to play important roles in necessary in the future to reveal a more complete picture reproduction, such as GnRH, GnIH, VIP, and AVT, are of the neuroendocrine control mechanism of avian synthesized in the brain nuclei of the hypothalamus. reproduction. Gonadotropin-releasing hormone, GnIH, and VIP are FIGURE 1.1 Generalized anatomical structure of the hypothalamus and pituitary in the midsagittal section of the avian brain. The hypothalamus is in the anterior part of the diencephalon, which is located between the telencephalon and midbrain (MB) (inset). Neuronal cell bodies with a common function often cluster in speciﬁc brain nuclei in the hypothalamus. The pituitary gland consists of the anterior pituitary including the pars distalis (PD) and pars tuberalis (PT), and the posterior pituitary (pars nervosa (PN)). There is either no pars intermedia in the adult avian pituitary, or it is highly reduced (Norris, 2007). AHA, anterior hypothalamic area; AHP, posterior hypotha- lamic area; CA, anterior commissure; CO, optic chiasm; IN, infundibular nucleus; ME, median eminence; MM, medial mammillary nucleus; NIII, nervus oculomotorius; POD, dorsal preoptic nucleus; POM, medial preoptic area; PVN, paraventricular nucleus; PVO, paraventricular organ; SC, supra- chiasmatic nucleus; TSM, septomesencephalic tract. Reconstructed from Stokes, Leonard, and Nottebohm (1974); Foster, Plowman, Goldsmith, and Follett (1987); Matsumoto and Ishii (1992).
Chapter | 1 Neuroendocrine Control of Reproduction in Birds 3 TABLE 1.1 Molecular structure and function of neurohormones controlling reproduction in birds Structure Species Function aGnRH-I pEHWSYGLQPG-NH2 (chicken, turkey, Chicken (King & Millar, 1982; Stimulation of LH and FSH release goose, dove, zebra ﬁnch, European Miyamoto et al., 1982; Dunn et al., (Millar & King, 1983; Hattori et al., starling) 1993); turkey (Kang et al., 2006); 1985) goose (Huang et al., 2008); dove (Mantei et al., 2008); zebra ﬁnch (Stevenson et al., 2009; Ubuka & Bentley, 2009); European starling (Sherwood et al., 1988; Stevenson et al., 2009; Ubuka et al., 2009) aGnRH-II pEHWSHGWYPG-NH2 (chicken) Chicken (Miyamoto et al., 1984) Stimulation of LH and FSH release (Hattori et al., 1986); stimulation of copulation solicitation (Maney et al., 1997b) GnIH SIRPSAYLPLRF-NH2 (chicken); Quail (Tsutsui et al., 2000; Satake Inhibition of LH and FSH release (Tsutsui SIKPSAYLPLRF-NH2 (quail); et al., 2001); white-crowned sparrow et al., 2000; Ciccone et al., 2004; Osugi SIKPFSNLPLRF-NH2 (white-crowned (Osugi et al., 2004); zebra ﬁnch et al., 2004; Bentley et al., 2006; Ubuka sparrow, zebra ﬁnch); SIKPFANLPLRF- (Tobari et al., 2010); European starling et al., 2006); inhibition of copulation NH2 (European starling) (Ubuka et al., 2008a) solicitation (Bentley et al., 2006) VIP HSDAVFTDNYSRFRKQMAVKKYLNSVLT- Chicken (Nilsson, 1975; Talbot et al., Stimulation of PRL release (Macnamee NH2 (chicken, turkey) 1995); turkey (You et al., 1995) et al., 1986; Opel & Proudman, 1988; Proudman & Opel, 1988) AVT CYIQNCPRG-NH2 (chicken, goose, Chicken (Acher et al., 1970); goose Induction of oviposition (Shimada et al., turkey, ostrich) (Acher et al., 1970); turkey (Acher 1986; Saito & Koike, 1992); stimulation ´ et al., 1970); ostrich (Rouille et al., of sexual behavior (Kihlstrom & ¨ 1986) Danninge, 1972; Maney et al., 1997a; Castagna et al., 1998; Goodson, 1998a; 1998b; Goodson & Adkins-Reagan, 1999) FSH, follicle-stimulating hormone; LH, luteinizing hormone; PRL, prolactin. thought to be transmitted through neuronal axons and 3. MECHANISMS AND PATHWAYS released into the portal vessels in the median eminence REGULATING GONADOTROPIN (GTH) (ME). Other mechanisms may exist to orchestrate the SECRETION actions of various neurohormones, such as direct inter- actions of neurohormones in the hypothalamus. Neuro- 3.1. Gonadotropin-releasing Hormone hormones released at the ME are directly conveyed to the (GnRH) anterior pituitary (adenohypophysis) in the blood and stimulate or inhibit anterior pituitary hormone secretion. Reproductive activities of vertebrates are primarily regu- Six adenohypophysial hormones have been identiﬁed in lated by hypothalamic GnRHs. This decapeptide was birds: LH, FSH, PRL, thyrotropin (TSH), corticotropin originally isolated from mammals (Matsuo, Baba, Nair, (ACTH), and growth hormone (GH) (Scanes, 1986). Arimura, & Schally, 1971; Burgus et al., 1972) and Hypothalamic neurohormones, such as AVT and meso- subsequently from chickens (King & Millar, 1982; Miya- tocin (MST), which are produced in magnocellular moto et al., 1982). The molecular structure of the originally neurons in the hypothalamus, are transmitted through isolated mammalian GnRH (mGnRH-I) is pEHW- their axons and released at the neural lobe of the pitui- SYGLRPG-NH2. Chicken GnRH-I (cGnRH-I) (pEHW- tary, which is called the posterior pituitary or pars nerv- SYGLQPG-NH2) differs by one amino acid from mGnRH-I osa (Oksche & Farner, 1974). Anterior pituitary hormones in that glutamine is substituted for arginine at position and hypothalamic neurohormones, which are released at eight. Speciﬁc genes encoding the same cGnRH-I peptide the posterior pituitary, travel in the general circulation have been identiﬁed by cDNA cloning in Galliformes and regulate the physiology and behavior of the bird. (chicken, quail, turkey) (Dunn, Chen, Hook, Sharp, &
4 Hormones and Reproduction of Vertebrates FIGURE 1.2 The neuroendocrine system controlling Environmental information (light, food availability, predation pressure etc.) reproduction of birds. Environmental information, such Social interactions (sight, sound, contact etc.) as light, food availability, predation pressure, and social interactions, are perceived by the brain. Hypothalamic neurohormones integrate external and internal signals to Thyroid Stress control pituitary function. The activity of gonadotropin- Melatonin hormone hormone inhibiting hormone (GnIH) is likely to be stimulated by the action of melatonin and stress. Gonadotropin-inhib- iting hormone may suppress reproductive activities of Brain birds by directly inhibiting gonadotropin (GTH) (lutei- nizing hormone (LH) and follicle-stimulating hormone aGnRH-I GnIH aGnRH-II (FSH)) secretion from the pars distalis (PD), or by inhibiting the actions of avian gonadotropin-releasing hormone (aGnRH-I and aGnRH-II) neurons. The stim- AVT Biological ulatory action of aGnRH-I on GTH secretion may be clock accelerated by the action of triiodothyronine (T3) on the T4 reduction of glial processes encasing aGnRH-I nerve VIP terminals at the median eminence. Triiodothyronine is converted from thyroxine (T4) by the action of DII, which DII T3 is induced by thyrotropin (TSH). Thyrotropin is synthe- sized in the pars tuberalis (PT) by photostimulation. LH TSH PRL Gonadotropins act on the gonads to induce steroidogen- FSH PT PD PD PN esis and gametogenesis. Sex steroids act on various organs including the brain to organize and activate sex Sexual behavior characteristics. Ovulation in females seems to occur by Aggression the synergistic actions of progesterone (P4), aGnRH-I, Gonads Courtship and LH. Cell bodies containing aGnRH-II are found in Sex steroid the midbrain. It is more likely that aGnRH-II regulates Copulation synthesis, release sexual behavior rather than stimulating GTH secretion. Spermatogenesis Oviposition The neurohypophysial hormone arginine vasotocin Oogenesis (AVT) produced in magnocellular neurons is released Ovulation Parental behavior from the pars nervosa (PN) to induce oviposition. Par- Incubation vocellular AVT neurons are likely to regulate various Feeding male sexual behaviors. Vasoactive intestinal peptide (VIP) is released at the median eminence (ME) to stim- ulate prolactin (PRL) release from the PD. Prolactin induces parental behaviors, such as incubation and feeding of the young. The seasonal reproductive cycle of birds is initiated by the interactions of biological clocks and neurohormones, the actions of which are modiﬁed by various external and internal signals. Sang, 1993; Kang et al., 2006), Anseriformes (goose, duck) (Norris, 2007; see also Volume 1, Chapter 2; Volume 2, (Huang, Shi, Z. Liu, Y. Liu, & Li, 2008), and Colum- Chapter 2; Volume 5, Chapter 2). The structure of cGnRH- biformes (dove) (Mantei, Ramakrishnan, Sharp, & Buntin, II (pEHWSHGWYPG-NH2) differs by three amino acids 2008). Although the existence of the same cGnRH-I from mGnRH-I or aGnRH-I at positions ﬁve, seven, and peptide was unknown in passerine birds for a long time, the eight. We will also refer to cGnRH-II as avian GnRH-II mRNA encoding cGnRH-I was recently identiﬁed in zebra (aGnRH-II) to be consistent with the naming of aGnRH-I. ﬁnches (Ubuka & Bentley, 2009; Stevenson, Lynch, Note that aGnRH-I and -II were formerly named cGnRH-I Lamba, Ball, & Bernard, 2009) and in European starlings and -II, respectively. (Ubuka, Cadigan, Wang, Liu, & Bentley, 2009; Stevenson Speciﬁc antibodies against avian GnRH peptides et al., 2009). The expression of cGnRH-I peptide in song- (aGnRH-I and aGnRH-II) have been made, and the histo- birds also has been suggested from its high-performance logical localization of aGnRHs has been studied in the liquid chromatography (HPLC) elution pattern and its chicken and quail (Mikami, Yamada, Hasegawa, & Miya- cross-reactivity with various GnRH antisera (Sherwood, moto, 1988; Van Gils et al., 1993). In mammals, the GnRH- Wingﬁeld, Ball, & Dufty, 1988). Accordingly, cGnRH-I I neurons originate at the olfactory placode and migrate to could be called avian GnRH-I (aGnRH-I) and we will use preoptic-septal nuclei during embryonic development this naming in this chapter. There is a second form of (Wray, Grant, & Gainer, 1989; Schwanzel-Fukuda & Pfaff, GnRH, which is called chicken GnRH-II (cGnRH-II). 1989). The migration of aGnRH-I neurons from the Chicken GnRH-II was ﬁrst found in chickens and subse- olfactory placode to the forebrain along the olfactory nerve quently in mammals (Miyamoto et al., 1984; King, Mehl, also has been observed in chickens (Norgren & Lehman, Tyndale-Biscoe, Hinds, & Millar, 1989; Morgan & Millar, 1991; Akutsu, Takada, Ohki-Hamazaki, Murakami, & Arai, 2004; Millar, 2005) and eventually in all vertebrate groups 1992; Yamamoto, Uchiyama, Ohki-Hamazaki, Tanaka, &
Chapter | 1 Neuroendocrine Control of Reproduction in Birds 5 Ito, 1996). In adult birds, aGnRH-I-immunoreactive (-ir) solicitation display, a female courtship behavior, in female cell bodies are found in a fairly wide area covering the white-crowned sparrows (Maney, Richardson, & Wing- hypothalamic preoptic area (POA) to the thalamic region. ﬁeld, 1997). On the other hand, magnocellular aGnRH-II-ir cell bodies Three GnRH receptor (GnRH-R) subtypes (types I, II, were found in the area dorsomedial to the nervus oculo- and III) have been identiﬁed, each with distinct distribu- motorius in the midbrain. Fibers immunoreactive for tions and functions in vertebrates (Millar et al., 2004). aGnRH-I or aGnRH-II were widely distributed in the These receptor subtypes belong to the G-protein-coupled telencephalon, diencephalon, and mesencephalon receptor (GPCR) superfamily. Two receptor subtypes have (midbrain). In sharp contrast to the existence of abundant been identiﬁed in chickens: type I (GnRH-R-I) (Sun et al., aGnRH-I-ir ﬁbers in the external layer of the ME, aGnRH- 2001a; 2001b) and type III (GnRH-R-III) (Shimizu & II-ir ﬁbers were absent or less prominent in this area, ´ ´ Bedecarrats, 2006), according to the classiﬁcation by suggesting that the major GnRH controlling pituitary Millar et al. (2004). GnRH-R-I is widely expressed, and function is aGnRH-I (Mikami et al., 1988; Van Gils et al., aGnRH-II has a higher binding afﬁnity to this receptor and 1993). is more potent in stimulating accumulation of inositol tri- Speciﬁc radioimmunoassays (RIAs) for chicken LH sphosphate, a secondary messenger molecule that can (Follett, Scanes, & Cunningham, 1972), turkey LH (Burke, induce GTH release, than aGnRH-I (Sun et al., 2001a; Licht, Papkoff, & Bona-Gallo, 1979), and chicken FSH 2001b). Inositol trisphosphate accumulation in response to (Scanes, Godden, & Sharp, 1977; Sakai & Ishii, 1980) have aGnRH-II binding to GnRH-R-III was also more marked been developed and used to measure the effect of GnRH on than in response to aGnRH-I. As fully processed GnRH-R- GTH release. The action of aGnRH-I on LH release from III mRNA was exclusively expressed in the pituitary, and its chicken anterior pituitary cells was ﬁrst shown in vitro mRNA level was positively correlated with reproductive (Millar & King, 1983). Subsequently, the activities of states in both sexes, it is likely that GnRH-R-III plays a role aGnRH-I on LH and FSH release was shown both in vivo in the regulation of GTH secretion by pituitary gonado- and in vitro in quail (Hattori et al., 1985). The activity of ´ ´ tropes (Shimizu & Bedecarrats, 2006). Despite the impli- aGnRH-I on LH release was more marked than that on FSH cation here that aGnRH-II is more effective in regulation of release both in vivo and in vitro (Hattori et al., 1985). The gonadotrope function, the current opinion is that aGnRH-I, activity of aGnRH-II (Miyamoto et al., 1984) on LH and and not aGnRH-II, is the dominant regulator of GTH FSH release was also shown in vivo and in vitro (Hattori, release. Ishii, & Wada, 1986). The activity of aGnRH-II on LH and FSH release was almost equal to that of aGnRH-I. Again, 3.2. Gonadotropin-inhibiting Hormone the activity of aGnRH-II on LH release was more marked (GnIH) than on FSH release both in vivo and in vitro. No synergism was observed between aGnRH-I and aGnRH-II on LH or A hypothalamic neuropeptide, GnIH, has been found to be FSH release in vitro (Hattori et al., 1986). an inhibiting factor for LH release from the quail anterior The physiological roles of aGnRH-I and aGnRH-II on pituitary (Tsutsui et al., 2000). Gonadotropin-inhibiting LH release also have been investigated in chickens (Sharp hormone-ir neuronal cell bodies are located in the para- et al., 1990). Egg laying of somatically mature hens is ventricular nucleus (PVN) in quail (Ubuka, Ueno, Ukena, regulated by strain differences and environmental condi- & Tsutsui, 2003; Ukena, Ubuka, & Tsutsui, 2003). These tions. As ovulation is controlled by the preovulatory LH neurons project to the ME, thus providing a functional surge (as described in Section 4.1), the activity of GnRH anatomical infrastructure that regulates anterior pituitary may be higher in laying hens. The amount of aGnRH-I in function. A cDNA encoding the GnIH precursor poly- the ME was higher in laying than in out-of-lay hens, as peptide has been cloned from the brains of quail (Satake measured by RIA. Avian GnRH-II was not detected in the et al., 2001), white-crowned sparrows (Osugi et al., 2004), ME. The amount of aGnRH-I in the hypothalamus European starlings (Ubuka et al., 2008a), and zebra increased in cockerels at the onset of puberty, but the ﬁnches (Tobari et al., 2010). The expression of GnIH amount of aGnRH-II did not change. Active immunization precursor mRNA also has been observed in the PVN of of laying hens against aGnRH-I but not against aGnRH-II these birds. resulted in the complete regression of the reproductive Gonadotropin-inhibiting hormone homologs are present system. Accordingly, it was concluded that GTH secretion in the brains of other vertebrates, such as mammals, in chickens is more likely to be controlled by aGnRH-I amphibians, and ﬁshes (Tsutsui & Ukena, 2006; Fukusumi, (Sharp et al., 1990). On the other hand, aGnRH-II may be Fujii, & Hinuma, 2006). These peptides, categorized as involved in the control of sexual behaviors in various RFamide-related peptides (RFRPs), possess a characteristic animals (Millar, 2003). Indeed aGnRH-II, but not LPXRF-amide (X ¼ L or Q) motif at their C-termini in all aGnRH-I, administered to the brain increased copulation vertebrates tested. Three LPXRF-amide (X ¼ L or Q)
6 Hormones and Reproduction of Vertebrates peptide sequences are encoded in the GnIH precursor To clarify the functional signiﬁcance of GnIH in the polypeptide, designated GnIH-related peptide-1 (GnIH-RP- control of avian reproduction, Ubuka, Ukena, Sharp, Bent- 1), GnIH, and GnIH-RP-2. Quail GnIH (SIKPSAYLPLRF- ley, and Tsutsui (2006) investigated the action of GnIH on amide), quail GnIH-RP-2 (SSIQSLLNLPQRF-amide), the hypothalamicepituitaryegonadal (HPG) axis in male starling GnIH (SIKPFANLPLRF-amide), and zebra ﬁnch quail. It is generally accepted that in avian species LH GnIH (SIKPFSNLPLRF-amide) have been identiﬁed as stimulates the formation of testosterone (T) by Leydig cells. mature endogenous peptides by mass spectrometric analyses Follicle-stimulating hormone and T stimulate growth, (Satake et al., 2001; Ubuka et al., 2008a, Tobari et al., 2010). differentiation, and spermatogenetic activity of the testis The receptor for quail GnIH has been identiﬁed and its (Follett, 1984; Johnson, 1986). Luteinizing hormone is binding activities have been investigated (Yin, Ukena, a protein complex, which is made of GTH common a and Ubuka, & Tsutsui, 2005). Structural analysis of the quail LHb subunits, whereas FSH is a complex of GTH common GnIH receptor revealed that it belongs to the GPCR a and FSHb subunits. Peripheral administration of GnIH to superfamily. A crude membrane fraction of COS-7 cells mature quail via osmotic pumps for two weeks decreased the transfected with the quail GnIH receptor cDNA speciﬁcally expression of GTH common a and LHb subunit mRNAs in bound GnIH, GnIH-RP-1, and GnIH-RP-2 in a concentra- the pituitary. Concentrations of plasma LH and T were also tion-dependent manner. The identiﬁed quail GnIH receptor decreased dose-dependently. Further, administration of mRNA was expressed in the pituitary as well as in various GnIH to mature birds induced testicular apoptosis and parts of the brain. The mammalian homolog of GnIH decreased spermatogenetic activity in the testis. In immature receptor is GPR147 (OT7T022, NPFF-1), and the mecha- birds, daily administration of GnIH for two weeks sup- nism of RFRP action on mammalian cellular events has pressed testicular growth and the rise in the concentration of been investigated (Fukusumi et al., 2006). RFamide-related plasma T. An inhibition of molt by juveniles also occurred peptides suppressed the production of cyclic-3’,5’-adeno- after GnIH administration. These results show that GnIH sine monophosphate (cAMP) in Chinese hamster ovarian may inhibit gonadal development and maintenance and also cells transfected with GPR147, suggesting that the receptor sexual development of birds by decreasing the synthesis and couples to the a-subunit of the inhibitory G-protein (Gai). release of GTHs (Ubuka et al., 2006). GPR147 mRNA is also expressed in various parts of the Although a dense population of GnIH neuronal cell mammalian brain as well as in the pituitary, suggesting that bodies was found only in the PVN, GnIH-ir ﬁbers were there are multiple actions of GnIH within the central widely distributed in the diencephalic and mesencephalic nervous system (Hinuma et al., 2000). regions in the Japanese quail (Ukena et al., 2003). Thus, it The actual release of GnIH into the hypothal- was hypothesized that GnIH may participate not only in the amusehypophysial portal system has not been reported in regulation of pituitary function, but also in behavioral and any vertebrate. However, the dense population of GnIH-ir autonomic mechanisms. Immunohistochemical studies ﬁbers in the ME in quail (Tsutsui et al., 2000; Ubuka et al., using light and confocal microscopy indicate that GnIH-ir 2003; Ukena et al., 2003), house sparrows and song sparrows axon terminals are in probable contact with aGnRH-I (Bentley, Perﬁto, Ukena, Tsutsui, & Wingﬁeld, 2003), and neurons in birds (Bentley et al., 2003). Thus, there is European starlings (Ubuka et al., 2008a) suggests a role for potential for the direct regulation of aGnRH-I neurons by GnIH in the regulation of pituitary function, at least in these GnIH neurons. Recently, Ubuka et al. (2008a) investigated birds. The same is true for white-crowned sparrows. The fact the interaction of GnIH and aGnRH-I neurons in the that GnIH inhibits release of GTHs from cultured quail and European starling brain. Double-label immunocytochem- chicken anterior pituitary provides strong support for this istry showed GnIH axon terminals on aGnRH-I and function (Tsutsui et al., 2000; Ciccone et al., 2004). aGnRH-II neurons (Bentley et al., 2003; Ubuka et al., Gonadotropin-inhibitory hormone administration to cultured 2008a). Further, in-situ hybridization of European starling chicken anterior pituitary inhibits not only the release of GnIH receptor mRNA combined with immunocytochem- GTHs but also the synthesis of GTH subunit mRNAs istry of aGnRHs showed the expression of GnIH receptor (Ciccone et al., 2004). Nevertheless, direct regulation of mRNA in both aGnRH-I and aGnRH-II neurons (Ubuka pituitary function by GnIH may be regulated in a different et al., 2008a). Central administration of GnIH inhibits the way in some bird species either developmentally or release of GTHs in white-crowned sparrows (Bentley et al., temporally because there is no apparent GnIH-ir material in 2006a) in a manner similar to peripheral administration of the ME in adult male Rufous-winged sparrows (Small et al., GnIH (Osugi et al., 2004; Ubuka et al., 2006). Accordingly, 2008), although GnIH receptor is expressed in the pituitary GnIH may inhibit the secretion of GTHs by decreasing gland in this species (McGuire, Ubuka, Perﬁto, & Bentley, aGnRH-I neuronal activity in addition to regulating the 2009). In other words, GnIH may directly inhibit pituitary release of pituitary GTHs directly. function only during certain periods before sexual matura- Central administration of GnIH also inhibits reproduc- tion or in response to stress, as described in Section 7. tive behavior of females in white-crowned sparrows
Chapter | 1 Neuroendocrine Control of Reproduction in Birds 7 (Bentley et al., 2006a). It is known that aGnRH-II enhances ten days) in a sequence (clutch), but the actual number copulation solicitation in estrogen-primed female white- varies greatly among species. Between the clutches there crowned sparrows exposed to male song (Maney et al., are one or more pause days. Generally clutch size is smaller 1997b). As a result of the putative contact of GnIH neurons and the interval between eggs is longer in species with aGnRH-II neurons in white-crowned sparrows producing large eggs. Many birds lay a ﬁxed number of (Bentley et al., 2003), Bentley et al. (2006a) investigated eggs in a clutch (determinate layers), but others can the effect of GnIH on copulation solicitation in females of continue laying for long periods (indeterminate layers) this species. Centrally administered GnIH inhibited copu- (Follett, 1984). Clutch size also tends to increase with lation solicitation in estrogen-primed female white- latitude (Ricklefs, 1970). crowned sparrows exposed to the song of males without In domestic chickens, ovulation occurs six to eight affecting locomotor activity. The result suggests that GnIH hours after the preovulatory LH surge and the egg spends inhibits reproductive physiology and behavior not only by about 24 hours in the oviduct before it is laid. The next inhibiting the secretion of GTHs from the pituitary but also ovulation occurs 15 to 75 minutes after the oviposition, by directly inhibiting aGnRH-I and -II neuronal activity except after the last oviposition in a clutch. As a result of within the brain (Ubuka, McGuire, Calisi, Perﬁto, & this temporal relationship, the time of oviposition is Bentley, 2008). a practical index of the time of ovulation. Under lightedark Many hormones that are classiﬁed as neuropeptides are cycles of 14L : 10D, chickens usually lay their eggs in the synthesized in vertebrate gonads in addition to the brain. ﬁrst half of the photophase whereas quail lay late in the day Recently, GnIH and its receptor were found to be expressed and early in the night. In both cases, the preovulatory surge in the gonads and accessory reproductive organs in Pass- of LH occurs six hours plus one day before the egg is laid. eriformes and Galliformes (Bentley et al., 2008). Immu- Under continuous light, the oviposition rhythms are free- nocytochemistry detected GnIH peptide in ovarian thecal running, and egg laying occurs throughout the 24 hours and granulosa cells, testicular interstitial cells and germ (Warren & Scott, 1936; Morris, 1961; Wilson & Cun- cells, and pseudostratiﬁed columnar epithelial cells in the ningham, 1981). Normally, the lightedark cycle entrains epididymis. Binding sites for GnIH were initially identiﬁed the rhythm, with dusk being the primary cue in chickens using in-vivo and in-vitro receptor ﬂuorography, and were (Bhatti & Morris, 1978a; 1978b) and dawn in Japanese localized in ovarian granulosa cells as well as in the quail (Tanabe, 1977). Other factors such as feeding, interstitial layer and seminiferous tubules of the testis. In- temperature changes, and bright/dim light are capable of situ hybridization of GnIH-R mRNA in testes produced entrainment when hens are illuminated constantly (Morris a strong reaction product that was localized to the germ & Bhatti, 1978). cells and interstitium. In the epididymis, the product was Ovulation depends on a surge of LH four to eight hours also localized in the pseudostratiﬁed columnar epithelial earlier, as determined by studies employing injection of LH cells. Similar data have been gathered from chickens, and or GnRH in intact birds or hypophysectomy (Fraps, 1970; estradiol (E2) and/or progesterone (P4) treatment of sexu- Van Tienhoven & Schally, 1972). A surge in plasma LH ally immature chickens signiﬁcantly decreased ovarian occurs four to eight hours before ovulation in chickens GnIH-R mRNA abundance (Maddineni, Ocon-Grove, ´ (Wilson & Sharp, 1973; Etches & Cunningham, 1977), Krzysik-Walker, Hendricks, Ramachandran, 2008). turkeys (Mashaly, Birrenkott, El-Begearmi, & Wentworth, Further, GnIH decreased LH-induced T release from 1976), and quail (Tanabe, 1977), and presumably other cultured dispersed testis (McGuire et al., 2009). The species. A constant relationship of about 30 hours exists distributions and action of GnIH and its receptor suggest between the peak of LH and the resulting oviposition, and a role for GnIH in autocrine/paracrine regulation of the LH peak is absent on the last day of a sequence. Plasma gonadal steroid production and possibly germ cell differ- FSH shows only minor changes during the ovulatory cycle entiation and maturation in birds. (Scanes et al., 1977), although there is a small increase 14 to 15 hours before ovulation. Prolactin levels appear to be inversely related to LH (Scanes, Chadwick, & Bolton, 4. MECHANISMS AND PATHWAYS 1976). REGULATING OVULATION AND As P4, but not estrogens, can induce premature ovula- OVIPOSITION tion in the hen, Fraps (1955; 1970) proposed that P4 triggers the preovulatory LH surge by a positive feedback mecha- 4.1. Regulation of Ovulation nism. A single major peak of P4 coincides with that of LH A hierarchy of developing follicles exists in the ovary of (Furr, Bonney, England, & Cunningham, 1973; Senior & birds, and the largest follicle is ovulated at regular intervals. Cunningham, 1974; Etches & Cunningham, 1977). This Many birds normally lay one egg each day during the peak is delayed by two to three hours each day in a laying breeding season. They usually lay two to ten eggs (two to sequence and is absent when no ovulation takes place.
8 Hormones and Reproduction of Vertebrates A preovulatory peak of E2 occurs with that of LH but Shimada, Neldon, & Koike, 1986) and decreases within 30 ovulation can take place in its absence (Lague, Van Tien- ¨ minutes of an egg being laid (Koike, Shimada, & Cornett, hoven, & Cunningham, 1975). The effects of various 1988). Elevation of plasma AVT at the time of oviposition steroids on the LH surge and ovulation have been tested. is accompanied by a depletion of AVT concentration in the Progesterone almost always triggers an LH surge that neurohypophysis (Sasaki, Shimada, & Saito, 1998). begins 15 to 45 minutes after intramuscular injection, peaks Magnocellular neurons producing AVT are found in the within two hours, and lasts for about six hours. Gonado- preoptic nucleus, the supraoptic nucleus, and the PVN of tropin-releasing hormone seems to relay the effect of P4 on the hypothalamus. A sexually dimorphic population of the LH surge, because anti-GnRH antibody administration parvocellular AVT neurons is observed from the medi- blocks the effect of P4 (Fraser & Sharp, 1978). Intra- ocaudal part of the preoptic region to the dorsolateral part hypothalamic injections of P4 also trigger ovulation (Ralph of the bed nucleus of stria terminalis in male birds, sug- & Fraps, 1960). In summary, the P4 surge appears to be gesting a role in the control of male sexual behaviors important for initiating ovulation. (Jurkevich & Grossmann, 2003). Effects of AVT on various The ovulated egg is captured by the ostium of the male reproductive behaviors, such as aggressive and oviduct. Fertilization and deposition of the ﬁrst layer of courtship behaviors, including song production, have been albumen occur here. The ovum passes down the oviduct documented (Kihlstrom & Danninge, 1972; Maney, Goode, ¨ through highly differentiated regions that have speciﬁc & Wingﬁeld, 1997; Castagna, Absil, Foidart, & Balthazart, functions. Further albumen is laid down in the magnum, 1998; Goodson, 1998a; 1998b; Goodson & Adkins-Regan, and membranes surround the developing egg in the 1999). There is also a role for AVT, along with cortico- isthmus. On reaching the shell gland (also known as the tropin-releasing hormone (CRH), in ACTH release from uterus), a shell and pigment are deposited (Solomon, 1983). the anterior pituitary (Castro, Estivariz, & Iturriza, 1986; Finally, oviposition occurs through the vagina and cloaca. Romero, Soma, & Wingﬁeld, 1998; Madison, Jurkevich, & Note that since there is only one ovary and one oviduct, Kuenzel, 2008). further ovulations cannot occur unless oviposition has occurred (Sharp, 1980). 5. MECHANISMS AND PATHWAYS 4.2. Regulation of Oviposition REGULATING PROLACTIN (PRL) Oviposition means expulsion of the egg from the oviduct to SECRETION the external environment and is a common phenomenon in A period of egg incubation occurs in the vast majority of vertebrates other than eutherian mammals. Avian oviposi- birds (Drent, 1975). Brood patches develop in virtually all tion is thought to be regulated by a neurohypophysial birds and seem to be used to transfer body heat to the eggs. hormone, AVT, together with ovarian hormones and pros- The changes in the brood pouch skin are substantial, taglandins (PGs) through the induction of uterine contrac- involving hyperplasia of the epidermis, an edema leading to tions (Munsick, Sawyar, & Van Dyke, 1960; Rzasa & Ewy, wrinkling of the skin, and extra vascularization. The whole 1970; Hertelendy, 1972; Wechsung & Houvenaghel, 1976; process is thought to be controlled by a synergism between Olson, Biellier, & Hertelendy, 1978; Toth, Olson, & Her- PRL and the sex steroids (Jones, 1971; Drent, 1975). telendy, 1979; Takahashi, Kawashima, Kamiyoshi, & Estrogens and P4 are the active agents in the female, but Tanaka, 1992). Regulation of oviposition by the sympa- where males incubate these are replaced by androgens. thetic nervous system using galanin as a neurotransmitter Injections of PRL induce chickens to incubate eggs seems to exist in quail (Li, Tsutsui, Muneoka, Minakata, & (Riddle, Bates, & Lahr, 1935; Sharp, Macnamee, Sterling, Nomoto, 1996; Tsutsui, Azumaya, Muneoka, Minakata, & Lea, & Pedersen, 1988), and maintain readiness of ring Nomoto, 1997; Tsutsui, Li, Ukena, Kikuchi, & Ishii, 1998; doves to incubate their clutches (Lehrman & Brody, 1964; Sakamoto et al., 2000). The expression of galanin in the Janik & Buntin, 1985). In species that hatch precocial sympathetic ganglia is regulated by ovarian sex steroids young, PRL levels rise slightly during egg-laying, but then (Ubuka, Sakamoto, Li, Ukena, & Tsutsui, 2001). increase markedly throughout incubation and fall imme- The neurohypophysial hormones AVT and MST repre- diately when the chicks have hatched. In female birds that sent the nonmammalian homologs to arginine vasopressin fail to incubate, as well as in males, PRL never rises above and oxytocin, respectively (Acher, Chauvet, & Chauvet, baseline concentrations (mallards (Goldsmith & Williams, 1970). However, in birds, the oxytocic effect of AVT is 1980)). In species that produce altricial young, PRL is also greater than that of MST (Saito & Koike, 1992; Barth et al., very high during incubation but it often stays high whilst 1997). Plasma AVT increases sharply at the time of the young are fed in the nest (canary (Goldsmith, 1982)). In oviposition to induce uterine contraction (Nouwen et al., ring doves and other Columbiformes, PRL causes growth 1984; Tanaka, Goto, Yoshioka, Terao, & Koga, 1984; of the crop gland and production of crop milk for feeding of
Chapter | 1 Neuroendocrine Control of Reproduction in Birds 9 young for the ﬁrst few days after hatch. In these birds, 6. MECHANISMS AND PATHWAYS plasma levels of PRL do not rise during egg-laying and the REGULATING SEASONAL REPRODUCTION early part of incubation but are high at the end of incubation and when the squabs are being fed (Goldsmith, Edwards, Koprucu, & Silver, 1981). It has been suggested that in 6.1. Seasonal Reproduction in Birds female turkeys the action of PRL on incubation behavior is Birds have presumably evolved the timing of their breeding facilitated by the combined action of E2 and P4 (El Hala- so that they can maximize the production of offspring, and wani, Silsby, Behnke, & Fehrer, 1986). laying is normally timed so that young are in the nest when In birds, PRL secretion is actively stimulated by release there is enough food for them to be raised (Lack, 1968). of VIP from the ME. Mammalian VIP speciﬁcally stimu- Baker (1938) suggested that seasonal breeding is controlled lated PRL release in vivo and in vitro in bantam hens by two sets of environment factors: ‘ultimate’ and ‘proxi- (Macnamee, Sharp, Lea, Sterling, & Harvey, 1986) and mate’ factors. The most important ultimate factor for birds turkeys (Opel & Proudman, 1988; Proudman & Opel, 1988), is the availability of an adequate food supply for the while immunohistochemical studies showed the presence of hatchlings as well as for the mother during the ﬁnal stages VIP-ir nerve terminals in the ME in quail (Yamada, Mikami, of ovarian development. Other ultimate factors operating in & Yanaihara, 1982), bantam hens (Macnamee et al., 1986), special situations are competition, nesting conditions, ´ and pigeons (Peczely & Kiss, 1988). The structure of predation pressure, and climate factors. However, these hypothalamic chicken and turkey VIP is regarded as the ultimate factors are often not those that trigger and regulate same as that isolated from the chicken gut, which is a 28- the secretion of reproductive hormones, because it is amino-acid peptide differing from mammalian VIP in four necessary to anticipate the hatching date and to begin amino acids (Nilsson, 1975). Both chicken and turkey VIP preparations for breeding some weeks or months ahead of cDNAs have been sequenced (Talbot, Dunn, Wilson, Sang, the time when young must be produced. & Sharp, 1995; You, Silsby, Farris, Foster, & El Halawani, In birds living in mid and high latitudes, there is 1995). Immunization against VIP inhibits PRL secretion in excellent experimental evidence that the annual change in bantam hens (Sharp, Sterling, Talbot, & Huskisson, 1989) day length controls the timing of breeding, and it may be and turkeys (El Halawani, Pitts, Sun, Silsby, & Sivanandan, assumed that photoperiod is a proximate factor for birds 1996). Daily injections of anti-VIP caused incubating living in such regions (Follett, 1984). Other environmental bantam hens to desert their nests. On the other hand, factors are also used to accelerate or retard photoperiodi- disruption of incubation behavior with anti-VIP was pre- cally induced gonadal growth (Farner & Follett, 1979). vented by concomitant administration of ovine PRL (Sharp These include the presence of males for stimulating ovarian et al., 1989). The amount of VIP was signiﬁcantly higher in development (Marshall, 1936; Hinde, 1965; Cheng, 1979), the ME and cell bodies in the medial basal hypothalamus in ambient temperature (Perrins, 1973), and rainfall (Leopold, incubating as compared to actively laying hens (Sharp et al., Erwin, Oh, & Browning, 1976). It is thought that photo- 1989). Vasoactive intestinal peptide mRNA and peptide period is not the proximate factor for many tropical and levels were low in nonphotostimulated turkeys, higher in desert species (Marshall, 1970). Reproduction of tropical laying hens, and highest in incubating hens. Changes in VIP birds, such as African stonechats (Gwinner & Scheuerlein, paralleled the changes in plasma PRL levels (Chaiseha, 1999) and zebra ﬁnches (Bentley, Spar, MacDougall- Tong, Youngren, & El Halawani, 1998). Dopaminergic Shackleton, Hahn, & Ball, 2000) can respond to changing control of PRL secretion also has been suggested in turkeys photoperiod although the experimental length of the (Youngren, Pitts, Phillips, & El Halawani, 1996; Youngren, photoperiods used in these studies exceeded that of the Chaiseha, & El Halawani, 1998). tropics. However, studies on spotted antbirds suggest that The peak in PRL concentrations coincides with tropical birds can respond to natural slight photoperiodic a decrease in LH concentrations and coincident gonadal changes (Hau, Wikelski, & Wingﬁeld, 1998; Beebe, regression in many bird species (Sharp & Sreekumar, Bentley, & Hau, 2005). The proximate factors used to time 2001), which suggests a role for PRL in the termination of breeding in tropical birds remain largely unknown although breeding. However, this is unlikely because administration correlative analyses suggest rainfall, territory, nest site of exogenous PRL does not on its own cause the onset of availability, nest materials, and food supply as being photorefractoriness (Goldsmith, 1985). Further, active involved (Immelmann, 1971; Zann, Morton, Jones, & immunization of starlings against VIP completely blocks Burley, 1995). Stonechats may respond to low light inten- PRL secretion but does not prevent gonadal regression sity as a predictive cue for rainfall (Gwinner & Scheuerlein, (Dawson & Sharp, 1998). The timing of high levels of PRL 1999). The reproductive axis of tropical birds may remain is also closely linked to molt, premigratory fattening, and in a state of ‘readiness to breed,’ and full functionality may migration (Meier & MacGregor, 1972; Meier, 1972; be triggered by the relevant proximate cues (Perﬁto, Dawson & Goldsmith, 1983). Bentley, & Hau, 2006; Perﬁto, Kwong, Bentley, & Hau,
10 Hormones and Reproduction of Vertebrates 2008). Although crossbills live in high latitudes, breeding photoperiods, but the timing can vary widely among indi- can occur opportunistically at any time between January viduals. If the photophase is decreased slightly, gonadal and August in response to their food supply. They feed on regression occurs sooner and is more synchronized among the seeds of coniferous trees, which are produced in individuals. Moreover, song sparrows can show renewed different amounts in different years, and at unpredictable gonadal maturation before exposure to short photoperiods times of the year. However, they have a short, ﬁxed (Wingﬁeld, 1993). nonbreeding period in fall when they appear to be photo- Seasonal changes in reproductive activities are corre- refractory (Hahn, 1998). lated with GTH secretion. The primary effect of long day The vast majority of temperate-zone passerines undergo lengths on stimulating GTH secretion has been shown in dynamic seasonal changes in their reproductive activities. quail (Follett, 1976), white-crowned sparrows (Wingﬁeld Gonadal development occurs in spring in response to & Farner, 1980), tree sparrows (Wilson & Follett, 1974), increasing day length (photostimulation). However, the canaries (Nicholls, 1974), ducks (Balthazart, Hendrick, & gonads are maintained in a functional condition only for Deviche, 1977), starlings (Dawson & Goldsmith, 1983), a short period, and they spontaneously regress after and many other birds. If male quail are transferred from extended exposure to long day lengths (absolute photo- short day lengths (8L : 16D) to long day lengths (20L : 4D), refractoriness). After becoming photorefractory, exposure the levels of FSH and LH rise substantially during the ﬁrst to short day length is required to regain photosensitivity week of photostimulation. Testicular growth and steroido- and thus allow for photostimulation (Wingﬁeld & Farner, genesis begin and maturity is reached in about ﬁve weeks 1980). Photorefractoriness seems to have evolved to (Follett & Robinson, 1980). Gonadal steroids affect GTH minimize the costs of reproducing in the rapidly deterio- secretion by negative feedback (King et al., 1989a; Dunn & rating environmental conditions of fall and winter (Follett, Sharp, 1999). Gonadal steroids also induce sexual behavior, 1984). The only well-studied birds that do not become development of secondary sexual characteristics, and photorefractory are some species of pigeon and dove spermatogenesis (Follett & Robinson, 1980). Female quail (Murton & Westwood, 1977). also grow their ovaries as a result of increased GTH A condition similar to absolute photorefractoriness is secretion induced by long day lengths (20L : 4D). Gonad- relative photorefractoriness. The main difference is that, otropin levels becomes basal after transferring quail from once relative photorefractoriness has been induced and the long days to short days (8L : 16D) (Gibson, Follett, & gonads have regressed, a subsequent substantial increase in Gledhill, 1975). On the other hand, in most of the day length will once more initiate reproductive temperate-zone passerine birds, which undergo sponta- maturationdwithout the need for a short-day-length neous photorefractoriness after exposure to long days, GTH ‘sensitization,’ or photosensitive, stage (Robinson & secretion is diminished and gonadal collapse occurs after Follett, 1982). For example, if Japanese quail experience a species-speciﬁc number of long days (Follett, 1984). day lengths of over 11.5 hours, rapid gonadal development Seasonality continues in the absence of the gonads. occurs. After about three months, and when (in the wild) Castrated or intact quail show an identical time-course in day length decreases below 14.5 hours, complete gonadal LH and FSH secretion under natural photoperiods over two regression occursdin a similar manner to absolute photo- consecutive years, the difference being that in summer the refractoriness (Nicholls, Goldsmith, & Dawson, 1988). GTH levels in castrated birds are higher, as a result of lack However, if the day length is subsequently artiﬁcially of negative feedback from gonadal steroids (Follett, 1984). increased further, a full return to reproductive maturity A similar annual cycle of LH secretion has been observed occurs. Indeed, if quail are maintained on any constant long in the plasma of intact and castrated white-crowned spar- day length, no form of photorefractoriness will be elicited rows (Mattocks, Farner, & Follett, 1976). It is also thought unless they experience a decrease in day length, e.g., from that gonads are not required for photorefractoriness to 23 to 16 hours (Nicholls et al., 1988). This suggests a shift develop, because castrated white-crowned sparrows in the critical day length in birds that are relatively (Wingﬁeld, Follett, Matt, & Farner, 1980), canaries (Storey, photorefractoryda shift that appears to depend on the Nicholls, & Follett, 1980), and starlings (Dawson & photoperiodic history of such birds (Robinson & Follett, Goldsmith, 1984) show a spontaneous fall in GTH level 1982). There does not seem to be any change in critical day under long days. Castration of photorefractory canaries length in birds that exhibit absolute photorefractoriness, does not cause enhanced LH secretion, but when photo- regardless of their photoperiodic history (Dawson, 1987). sensitivity is regained under short days there is an imme- Song sparrows and house sparrows show character- diate rise in plasma LH (Nicholls & Storey, 1976). istics of both absolute and relative photorefractoriness Birds seem to measure daylength using their circadian (Dawson, King, Bentley, & Ball, 2001). Song sparrows clock. In a classic experiment, white-crowned sparrows (Wingﬁeld, 1983) and house sparrows (Dawson, 1998a) held on short day lengths (8L : 16D) were placed in eventually become photorefractory during exposure to long continuous darkness. When birds were exposed to a single
Chapter | 1 Neuroendocrine Control of Reproduction in Birds 11 eight-hour photophase, an increase in LH occurred only if during the ﬁrst six weeks of photostimulation in female the photophase coincided with a time period 12e20 hours starlings. However, by 12 weeks after the onset of photo- after the subjective dawn, as judged by the circadian stimulation, as birds became photorefractory, GnRH had rhythms of the birds (Follett, Mattocks, & Farner, 1974). decreased to levels signiﬁcantly lower than those before These data imply that a circadian rhythm of sensitivity to photostimulation (Dawson, Follett, Goldsmith, & Nicholls, light, or photoinducibility, exists in the photoperiodic time 1985). Immunocytochemistry with quantitative image measurement system of these birds. There are two possible analyses for both GnRH and its precursor, proGnRH-GAP, models of how circadian rhythms might be involved in was performed after a photoperiodically induced repro- photoperiodic time measurement in birds (Goldman, 2001). ductive cycle in male starlings (Parry, Goldsmith, Millar, & The ‘external coincidence model’ assumes the organism Glennie, 1997). The size of cells staining for GnRH and possesses a circadian rhythm of ‘photosensitivity’. If proGnRH-GAP increased during gonadal maturation. A coincidence between this rhythm and light occurs under reduction in the number of cells staining for GnRH and the long days, it induces GTH secretion. The ‘internal coinci- size of cells staining for both GnRH and proGnRH-GAP dence model’ assumes the induction to occur when coin- occurred during gonadal regression, though staining for cidence is established between two separate circadian GnRH and proGnRH-GAP in the ME remained high. oscillators (usually dawn and dusk oscillators). As Staining for GnRH and proGnRH-GAP was reduced a consequence of using a circadian clock for photoperiodic signiﬁcantly after gonadal regression. These observations time measurement, light is not required throughout the day suggest that photorefractoriness is promoted by a reduction to induce gonadal growth, but pulses of light simulating in pro-GnRH-GAP and GnRH synthesis (Parry et al., dawn and dusk can cause induction if one of the pulses 1997). Changes in aGnRH-I in the POA and mediobasal coincides with the phase of photosensitivity (Follett, 1973). hypothalamus (MBH) including the ME have been As with white-crowned sparrows, when 15-minute pulses measured in starlings during the recovery of photosensi- of light were given at different times in the night to quail on tivity under short days, and following photostimulation at the basic photoperiod of 6L : 18D, induction occurred only various times during the recovery of photosensitivity if the pulses were within 12 to 16 hours of dawn (Follett & (Dawson & Goldsmith, 1997). During exposure of long- Sharp, 1969). day photorefractory starlings to short days for 10 days, Light intensity can also modify the reproductive there was a signiﬁcant increase in aGnRH-I in the POA but responses of birds under the same photoperiod (Bisson- not in the MBH. Photostimulation after 20 short days nette, 1931; Bartholomew, 1949). In the experiment con- caused an immediate increase in aGnRH-I in the POA, ducted by Bentley, Goldsmith, Dawson, Briggs, and a delayed increase in the MBH, but no increase in plasma Pemberton (1998), photosensitive starlings transferred LH. Photostimulation after 30 short days caused an from short days to long days of different light intensities immediate increase in aGnRH-I in the POA and the MBH underwent graded reproductive responses according to the and in plasma LH. These results show that the recovery of light intensities they experienced. Interestingly, the photosensitivity is gradual and the ﬁrst measurable change responses observed, such as the growth in their testes size occurs in the POA, consistent with photosensitivity being and the development of photorefractoriness, were similar to due to renewed aGnRH-I synthesis (Dawson & Goldsmith, those seen in starlings exposed to different photoperiods. At 1997). Recently, the complete sequence of aGnRH-I face value, these data contradict the external coincidence precursor mRNA was identiﬁed in songbirds: starlings model in that light falling in the photoinducible phase (Ubuka et al., 2009; Stevenson et al., 2009) and zebra should cause a long-day response. However, this discrep- ﬁnches (Ubuka & Bentley, 2009; Stevenson et al., 2009). ancy might be explained by the possibility that low light The expression of aGnRH-I precursor mRNA was found to intensities only weakly entrain the circadian oscillations of be regulated as a function of age and reproductive condition the photoinducible phase, so that light is experienced in in zebra ﬁnches (Ubuka & Bentley, 2009). In starlings, only part of the photoinducible phase. there was regulation of aGnRH-I precursor mRNA expression as a function of season (Ubuka et al., 2009) and photoperiod (Stevenson et al., 2009). Photostimulation of 6.2. Seasonal Changes in Gonadotropin- short-day-exposed chickens and turkeys can also increase aGnRH-I precursor mRNA expression (Dunn & Sharp, releasing Hormone (GnRH) 1999; Kang et al., 2006). Radioimmunoassay and immunocytochemistry (ICC) What is the molecular mechanism regulating aGnRH-I using GnRH antisera have numerous times demonstrated synthesis and release? Is GTH secretion solely controlled cyclic changes in GnRH in songbirds in response to by aGnRH-I? If photoperiod is the proximate factor changing photoperiod. Radioimmunoassay revealed that controlling seasonal reproduction, how is the photoperiodic hypothalamic GnRH content did not increase signiﬁcantly information acquired and processed in the brain?
12 Hormones and Reproduction of Vertebrates Photoreceptors to perceive light and a biological clock to been controversy concerning the precise location of the process photoperiodic information seem necessary to time avian homologs of the mammalian SCN. The medial seasonal reproduction. How autonomous are the seasonal hypothalamic nucleus (MHN) (also termed the medial reproductive activities? In other words, does external SCN) and the lateral hypothalamic retinorecipient nucleus information such as day length need to be sensed through (LHRN) (also termed the visual SCN) are the possible the whole year to time seasonal reproduction? Does the homologs of the mammalian SCN (Norgren & Silver, 1989; daily melatonin (MEL) rhythm control reproductive cycles 1990; Shimizu, Cox, Karten, & Britto, 1994; Cassone & of birds? Thyroid hormones seem to be required to achieve Moore, 1987). seasonal reproduction, but what is the mechanism The self-sustaining circadian oscillation in any involved? Studies on the potential mechanisms controlling organism is thought to be generated by a tran- seasonal reproduction of birds will be discussed in the scriptionetranslation feedback loop of clock genes, the following sections. presence of which appears to be a conserved property from fruit ﬂies to humans. Clock and Period homologs (qClock, qPer2, and qPer3) have been cloned in the Japanese quail. 6.3. Photoreceptor qPer2 and qPer3 showed robust circadian oscillations in the It is believed that light can affect the activity of birds via eye and in the pineal gland, although qClock mRNA was three different pathways: the eyes, the pineal, and the deep expressed throughout the day. In addition, qPer2 mRNA brain (Underwood, Steele, & Zivkovic, 2001). The avian was induced by light, whereas qClock or qPer3 were not eye is not only a functional photoreceptor, but also contains (Yoshimura et al., 2000). These clock genes were expressed a circadian clock and produces a circadian rhythm of MEL in the MHN, but not in the LHRN in quail (Yoshimura release (Binkley, Reilly, & Hryschchyshyn, 1980; Hamm & et al., 2001). On the other hand, Per2 mRNA is expressed Menaker, 1980). The principal cell types within the pineal both in the MHN and in the LHRN with rhythmic expres- of most nonmammalian vertebrates have characteristics of sion patterns in the house sparrow (Abraham, Albrecht, a photosensory cell, including the presence of an outer Gwinner, & Brandstatter, 2002). Clock genes such as Per, ¨ segment composed of stacked disks containing photopig- Cry, Clock, Bmal, and E4bp4 are all expressed and differ- ments (Collin & Oksche, 1981). The avian pineal organ is entially oscillate in quail and chicken pineal glands (Doi, directly photosensitive and it is also the locus of a circadian Nakajima, Okano, & Fukada, 2001; Okano et al., 2001; pacemaker (Takahashi & Menaker, 1984; Okano & Fukada, Yamamoto, Okano, & Fukada, 2001; Fukada & Okano, 2001). The location of the extrapinealeextraretinal photo- 2002; Yasuo, Watanabe, Okabayashi, Ebihara, & Yoshi- receptors mediating circadian entrainment in birds has not mura, 2003). The avian pineal gland seems to possess been established. In a study using opsin antibodies, cere- a functional circadian oscillator composed of a transcrip- brospinal ﬂuid-contacting cells were labeled in the septal tion-/translation-based autoregulatory feedback loop, as in and the tuberal areas in the ring dove (Silver et al., 1988), the mammalian SCN (Fukada & Okano, 2002). Thus, and lateral septum in the pigeon (Wada, Okano, & Fukada, multiple oscillators are present in birds, and they are 2000). Light and confocal microscopy revealed interactions somehow coordinated to convey circadian rhythmicity. of GnRH-ir and opsin-ir materials in the POA and in the Annual seasonal activities of birds, such as reproduction, ME, suggesting a direct communication between these molt, and migration, can persist for many cycles, with putative deep brain photoreceptors and GnRH neurons a period deviating from 12 months under constant condi- (Saldanha, Silverman, & Silver, 2001). tions. These cycles have been named ‘circannual rhythms’ (Gwinner, 2003), although many of them deviate signiﬁ- cantly from a 12-month period. These cycles have been 6.4. Biological Clock experimentally demonstrated for at least 20 species of bird The circadian system of birds is composed of several under speciﬁc lighting conditions (Gwinner, 1986; Gwinner interacting sites, including the pineal organ, the supra- & Dittami, 1990; C. Guyomarc’h & J. Guyomarc’h, 1995). chiasmatic nucleus (SCN) of the hypothalamus, and eyes, In European starlings, a cycle of reproduction composed of in at least some species. Each of these sites may contain photosensitive and photorefractory phases continues in a circadian clock (Underwood et al., 2001). Signiﬁcant constant photoperiods close to 12 hours (Gwinner, 1996; variation can occur among birds in the relative roles that the Dawson, 1997). Under photoperiods longer than 12 hours, pineal, the SCN, and the eyes play within the circadian starlings remain in the photorefractory state, whereas under system. For example, in the house sparrow, circadian shorter photoperiods they remain in the photosensitive state pacemakers in the pineal play the predominant role, (Gwinner, 1996). Castrated starlings exposed to 12L : 12D whereas in the pigeon circadian pacemakers in both the did not exhibit cyclic rhythms of this type (Dawson & pineal and eyes play a signiﬁcant role. In Japanese quail, McNaughton, 1993). Accordingly, the reproductive cycle ocular pacemakers play the predominant role. There has that was observed for intact birds under this speciﬁc