Hormones and Reproduction of Vertebrates, Volume 4: Birds

By David Norris and Kristin Lopez

This series of volumes represents a comprehensive and integrated treatment of reproduction in vertebrates from fishes of all sorts through mammals. It is designed to provide a readable, coordinated description of reproductive basics in each group of vertebrates as well as an introduction to the latest trends in reproductive research and our understanding of reproductive events. Whereas each chapter and each volume is intended to stand alone as a review of that topic or vertebrate group, respectively, the volumes are prepared so as to provide a thorough topical treatment across the vertebrates. Terminology has been standardized across the volumes to reduce confusion where multiple names exist in the literature, and a comprehensive glossary of these terms and their alternative names is provided.

• A complete, essential and up to date reference for research scientists working on vertebrate hormones and reproduction - and on animlals as models in human reproductive research
• Covers the endocrinology, neuroendocrinology, physiology, behaviour and anatomy of vertebrate reproduction
• Structured coverage of the major themes for all five vertebrate groups allows a consistent treatment for all
• Special chapters elaborate on features specific to individual vertebrate groups and to comparative aspects, similarities and differences between them

• Language: English
• Publisher: Academic Press
• Release date: May 4, 2011
• ISBN: 9780080958057

Book preview

Table of Contents

Cover image

Front Matter

Copyright

Dedication

Preface

Preface

Contributors

Chapter 1. Neuroendocrine Control of Reproduction in Birds

1. Introduction

2. The Hypothalamus–Pituitary System (HPS)

3. Mechanisms and Pathways Regulating Gonadotropin (GTH) Secretion

4. Mechanisms and Pathways Regulating Ovulation and Oviposition

5. Mechanisms and Pathways Regulating Prolactin (PRL) Secretion

6. Mechanisms and Pathways Regulating Seasonal Reproduction

7. Future Research Directions

Chapter 2. Avian Testicular Structure, Function, and Regulation

1. Central Mechanisms Regulating Testicular Development

2. Endocrine Influence on Development of The Avian Male Phenotype

3. Avian Testicular Anatomy

4. Endocrine and Exocrine Functions of Avian Testes

5. Endocrine and Paracrine Control of Avian Testicular Function

6. Exogenous Regulation of Testicular Function

7. Ecology of Testicular Functions

8. Testicular Dysfunction

9. Anthropogenic Effects on Testicular Function

10. Conclusions and Future Directions

Chapter 3. Organization and Functional Dynamics of the Avian Ovary

1. The Avian Ovary

2. Developmental Dynamics and Organization of The Avian Ovary

3. Reproductive Seasonality

4. Follicular Development

5. Summary

Chapter 4. Maternal Hormones in Avian Eggs

1. Introduction: importance of the topic and outline

2. Hormones and levels

3. Mechanisms of accumulation

4. Effects on offspring

5. Mechanisms of action

6. Functional and evolutionary aspects

7. Conclusion, GAPS, and perspectives

Chapter 5. Stress and Reproduction in Birds

1. Introduction

2. Regulation of Glucocorticoid (GC) Secretion

3. Intermediate Performance Measures

4. Direct Fitness Metrics

5. Summary

Chapter 6. Hormonal Regulation of Avian Courtship and Mating Behaviors

1. Introduction

2. Steroid hormones synchronize courtship and mating behaviors with reproductive physiology and environmental factors

3. Steroid hormones act within distinct brain regions to influence courtship and mating

4. Steroid hormone synthetic enzymes and metabolites in the brain

5. Neuroendocrine regulation of male sexual behavior

6. Neuroendocrine regulation of female sexual behavior

7. Closing remarks

Chapter 7. Hormones and Regulation of Parental Behavior in Birds

1. Introduction

2. Nest building

3. Incubation

4. Care of young

5. Testosterone (T) and male parental behavior

6. Effects of environmental stress on parental behavior—roles of corticosterone (CORT) and prolactin (PRL)

7. Special cases of parental behavior

8. Future research

Chapter 8. Hormones in Migration and Reproductive Cycles of Birds

1. Introduction

2. Life history and ecology of the subspecies of the white-crowned sparrow (zonotrichia leucophrys)

3. Hypothalamic–pituitary control of hormones in the reproductive cycles of male and female birds

4. Annual cycles of migratory and sedentary white-crowned sparrows

5. Applying finite state machine theory to migration and breeding

6. Timing migration and breeding cycles

7. The vernal migratory stage

8. The breeding life-history stage

9. The autumn migratory stage

10. Conclusions

11. Future directions

Chapter 9. Endocrine Disruption of Reproduction in Birds

1. Introduction

2. Impacts of endocrine-disrupting chemicals (EDCs)

3. Modes of exposure in birds

4. Challenges in assessing endocrine-disrupting chemical (EDC) effects in birds

5. Discerning the effects of different classes of endocrine-disrupting chemicals (EDCs)

6. Lifecycle and species differences in the timing of vulnerability to endocrine-disrupting chemicals (EDCs)

7. Major effects of endocrine-disrupting chemicals (EDCs) in avian species

8. Other considerations: effects of endocrine-disrupting chemicals (EDCs) on immune function and stress responses

9. Conclusions

Color Plates

Index

Index

Front Matter

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

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Copyright

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Dedication

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Richard Evan Jones

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 contributed to these volumes.

Preface

Hormones and Reproduction of Vertebrates Preface to the Series

Every aspect of our physiology and behavior is either regulated directly by hormones or modified by their actions, as exemplified by the essential and diverse roles of hormones in reproductive processes. Central to the evolutionary success of all vertebrates are the regulatory chemicals secreted by cells that control sexual determination, sexual differentiation, sexual maturation, reproductive physiology, and reproductive behavior. To understand these processes and their evolution in vertebrates, it is necessary to employ an integrated approach that combines our knowledge of endocrine systems, genetics and evolution, and environmental factors in a comparative manner. In addition to providing insight into the evolution and physiology of vertebrates, the study of comparative vertebrate reproduction has had a considerable impact on the biomedical sciences and has provided a useful array of model systems for investigations that are of fundamental importance to human health. The purpose of this series on the hormones and reproduction of vertebrates is to bring together our current knowledge of comparative reproductive endocrinology in one place as a resource for scientists involved in reproductive endocrinology and for students who are just becoming interested in this field.

In this series of five volumes, we have selected authors with broad perspectives on reproductive endocrinology from a dozen countries. These authors are especially knowledgeable in their specific areas of interest and are familiar with both the historical aspects of their fields and the cutting edge of today’s research. We have intentionally included many younger scientists in an effort to bring in fresh viewpoints. Topics in each volume include sex determination, neuroendocrine regulation of the hypothalamus–pituitary–gonadal (HPG) axis, separate discussions of testicular and ovarian functions and control, stress and reproductive function, hormones and reproductive behaviors, and comparisons of reproductive patterns. Emphasis on the use of model species is balanced throughout the series with comparative treatments of reproductive cycles in major taxa.

Chemical pollution and climate change pose serious challenges to the conservation and reproductive health of wildlife populations and humans in the twenty-first century, and these issues must be part of our modern perspective on reproduction. Consequently, we have included chapters that specifically deal with the accumulation of endocrine-disrupting chemicals (EDCs) in the environment at very low concentrations that mimic or block the critical functions of our reproductive hormones. Many authors throughout the series also have provided information connecting reproductive endocrinology to species conservation.

The series consists of five volumes, each of which deals with a major traditional grouping of vertebrates: in volume order, fishes, amphibians, reptiles, birds, and mammals. Each volume is organized in a similar manner so that themes can be easily followed across volumes. Terminology and abbreviations have been standardized by the editors to reflect the more common usage by scientists working with this diverse assembly of organisms we identify as vertebrates. Additionally, we have provided indices that allow readers to locate terms of interest, chemicals of interest, and particular species. A glossary of abbreviations used is provided with each chapter.

Finally, we must thank the many contributors to this work for their willingness to share their expertise, for their timely and thoughtful submissions, and for their patience with our interventions and requests for revisions. Their chapters cite the work of innumerable reproductive biologists and endocrinologists whose efforts have contributed to this rich and rewarding literature. And, of course, our special thanks go to our editor, Patricia Gonzalez of Academic Press, for her help with keeping us all on track and overseeing the incorporation of these valuable contributions into the work.

David O. Norris and Kristin H. Lopez

Preface

Preface to Volume 4 Birds

Birds are unique among vertebrates in that they are highly adapted for flight in terms of their anatomy, physiology, and behavior. Further, they are possibly the most visible vertebrate species to humans in being strongly diurnal, often brightly colored, and extremely easy to observe in their natural habitats. Consequently, birds have been a favorite target for biologists interested in studying the relationships among hormones, natural environmental factors, and reproduction in wild vertebrates.

Distributed in a wide range of habitats globally, all birds are characterized physiologically by endothermy, internal fertilization, and obligate oviparity. Females produce relatively small numbers of large yolky eggs, and embryonic development generally requires elevated temperatures, provided by brooding. Thus, considerable parental care is involved in the successful reproduction of most bird species.

This avian volume on hormones and reproduction focuses both on bird species in wild populations and on captive birds, in which reproductive physiology and behavior may be studied relatively easily. We begin with a chapter on the neuroendocrine regulation of reproduction and follow with chapters on testicular and ovarian functions. Following is a discussion of the maternal role in determining the hormonal and nutrient composition of the egg and its significance for successful reproduction. Chapters on the hormones involved in stress, courtship and mating behavior, parental behavior, and migration and reproductive cycles represent the emphases of the study of bird reproduction over the past several decades. Finally, the importance of endocrine disruption in bird populations by anthropogenic chemicals is discussed.

Contributors

Sarah J. Alger

University of Wisconsin, Madison, WI, USA

George E. Bentley

University of California at Berkeley, Berkeley, CA, USA

Creagh W. Breuner

University of Montana, Missoula, MT, USA

Karen Dean

Pierre Deviche

Arizona State University, Tempe, AZ, USA

H. Bobby Fokidis

Arizona State University, Tempe, AZ, USA

Ton G.G. Groothuis

University of Groningen, Haren, The Netherlands

Laura L. Hurley

Arizona State University, Tempe, AZ, USA

A.L. Johnson

The Pennsylvania State University, University Park, PA, USA

Moira McKernan

Mary Ann Ottinger

University of Maryland, College Park, MD, USA

Michael J. Quinn Jr.

Marilyn Ramenofsky

University of California, Davis, CA, USA

Takayoshi Ubuka

University of California at Berkeley, Berkeley, CA, USA

Lauren V. Riters

University of Wisconsin, Madison, WI, USA

Carol M. Vleck

Iowa State University, Ames, IA, USA

David Vleck

Iowa State University, Ames, IA, USA

Nikolaus von Engelhardt

University of Bielefeld, Bielefeld, Germany

Chapter 1. Neuroendocrine Control of Reproduction in Birds

Takayoshi Ubuka and George E. Bentley

University of California at Berkeley, Berkeley, CA, USA

SUMMARY

Reproductive physiology and behavior of birds are ultimately controlled by the hypothalamus–hypophysial system. Hypothalamic neurons integrate internal and external signals, controlling reproduction by releasing neurohormones to the adenohypophysis (anterior pituitary). Reproductive activation occurs via gonadotropin-releasing hormone (GnRH) stimulation of adenohypophysial gonadotropin secretion. Gonadotropins (GTHs) (luteinizing hormone (LH), follicle-stimulating hormone (FSH)) act on the gonads to stimulate gametogenesis and sex steroid production. Gonadotropin-inhibiting hormone (GnIH) may inhibit gonadotropin secretion directly or indirectly by decreasing the activity of GnRH neurons. Another adenohypophysial hormone that plays an important role in avian reproduction is prolactin (PRL). The secretion of PRL is thought to be regulated by a hypothalamic neuropeptide, vasoactive intestinal peptide. Arginine vasotocin (AVT) is released from the neurohypophysis (posterior pituitary) and regulates oviposition by directly inducing uterine contraction. Several mechanisms are discussed in terms of how the brain perceives and translates external environmental information into internal hormonal signals to time seasonal reproduction.

1. Introduction

Birds (class Aves) are bipedal, homeothermic oviparous vertebrate animals. Modern birds—comprising nearly 10 000 living species—are divided basally into two clades, Palaeognathae and Neognathae (Harshman, 2006). Palaeognathae includes the ratites (e.g. ostrich (Struthio camelus), emu (Dromaius novaehollandiae), and kiwis (Apteryx)) and tinamous. Neognathae is divided into Galloanserae and Neoaves. Galloanserae consist of the sister orders Anseriformes (e.g., ducks, geese, and swans) and Galliformes (e.g., turkeys, grouse, chickens, quail, and pheasants). Neoaves consist of 24 orders, including Columbiformes (pigeons, doves) and Passeriformes. Passeriformes include all songbirds, and contain more than half of all bird species (Sibley & Monroe, 1990).

Reproductive activities of birds consist of multiple stages in their life history. Typically, males establish territories after the initiation of gonadal maturation and form pairs with females. Male and female birds mature their gonads and engage in courtship, construct nests, and copulate, and female birds ovulate and lay eggs. After incubating their eggs, they feed nestlings and fledglings. Finally, the reproductive system regresses and the next life-history stage follows, e.g., molt (Wingfield et al., 1999). Many passerine species that breed at high latitudes incorporate two migratory periods between nonbreeding and breeding stages (Wingfield & Farner, 1980).

Reproductive physiology and behavior of birds are governed by the hypothalamic (neuroendocrine) control of pituitary hormone secretion (hypothalamus–pituitary system (HPS)). Accordingly, this chapter will start with a brief summary of the anatomy of the HPS and the neurohormones involved in avian reproduction. Gonadotropins (GTHs) (luteinizing hormone (LH), follicle-stimulating hormone (FSH)) are important anterior pituitary hormones that control avian reproduction by inducing gametogenesis (spermatogenesis, oogenesis) and sex steroidogenesis (androgens, estrogens, progestogens) in the gonad. Accordingly, investigation of how the hypothalamic neurohormones control GTH secretion from the pituitary is imperative to understand the neuroendocrine control of reproduction. Two hypothalamic neuropeptides, gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH), which have opposite effects on GTH secretion, will be introduced. Ovulation and egg-laying (oviposition) are highly orchestrated female reproductive actions that involve various hormones. Another hypothalamic neurohormone, arginine vasotocin (AVT), is released directly from the neurohypophysis and induces oviposition. After oviposition, incubation of the eggs and feeding of the offspring are the typical next stages in avian life history. These parental behaviors seem to be controlled by another anterior pituitary hormone, prolactin (PRL). Hypothalamic vasoactive intestinal peptide (VIP) is thought to regulate PRL secretion from the anterior pituitary. Many birds reproduce seasonally. How do birds perceive and translate external environmental information into internal hormonal signals to time reproduction? If reproductive physiology and behavior of birds are ultimately controlled by the HPS, how does this system control seasonal reproductive activities of birds? Does the hypothalamus detect the external environmental signals itself, or are they detected by other organs and the information transduced to the hypothalamic neuronal system to control pituitary hormone secretion? These interesting topics will be discussed in Section 3. Finally, we will investigate the lines of research that will be necessary in the future to reveal a more complete picture of the neuroendocrine control mechanism of avian reproduction.

2. The Hypothalamus–Pituitary System (HPS)

Reproductive activity of birds is controlled by the HPS. Hypothalamic neurons somehow integrate external (light, temperature, sound, etc.) and internal (water, nutrition, hormones, etc.) information, and regulate the reproductive physiology and behavior of the bird by releasing neurohormones to the pituitary. Figure 1.1 shows the generalized anatomical structure of the hypothalamus and pituitary in the avian brain (Stokes et al., 1974, Foster et al., 1987 and Matsumoto and Ishii, 1992). Table 1.1 summarizes the molecular structures and the known functions of the identified key neurohormones that control reproduction in birds. The neuroendocrine system controlling reproduction of birds is summarized in Figure 1.2. Various neurohormones that seem to play important roles in reproduction, such as GnRH, GnIH, VIP, and AVT, are synthesized in the brain nuclei of the hypothalamus. Gonadotropin-releasing hormone, GnIH, and VIP are thought to be transmitted through neuronal axons and released into the portal vessels in the median eminence (ME). Other mechanisms may exist to orchestrate the actions of various neurohormones, such as direct interactions of neurohormones in the hypothalamus. Neurohormones released at the ME are directly conveyed to the anterior pituitary (adenohypophysis) in the blood and stimulate or inhibit anterior pituitary hormone secretion. Six adenohypophysial hormones have been identified in birds: LH, FSH, PRL, thyrotropin (TSH), corticotropin (ACTH), and growth hormone (GH) (Scanes, 1986). Hypothalamic neurohormones, such as AVT and mesotocin (MST), which are produced in magnocellular neurons in the hypothalamus, are transmitted through their axons and released at the neural lobe of the pituitary, which is called the posterior pituitary or pars nervosa (Oksche & Farner, 1974). Anterior pituitary hormones and hypothalamic neurohormones, which are released at the posterior pituitary, travel in the general circulation and regulate the physiology and behavior of the bird.

3. Mechanisms and Pathways Regulating Gonadotropin (GTH) Secretion

3.1. Gonadotropin-releasing Hormone (GnRH)

Reproductive activities of vertebrates are primarily regulated by hypothalamic GnRHs. This decapeptide was originally isolated from mammals (Matsuo et al., 1971 and Burgus et al., 1972) and subsequently from chickens (King and Millar, 1982 and Miyamoto et al., 1982). The molecular structure of the originally isolated mammalian GnRH (mGnRH-I) is pEHWSYGLRPG-NH 2. Chicken GnRH-I (cGnRH-I) (pEHWSYGLQPG-NH 2) differs by one amino acid from mGnRH-I in that glutamine is substituted for arginine at position eight. Specific genes encoding the same cGnRH-I peptide have been identified by cDNA cloning in Galliformes (chicken, quail, turkey) (Dunn et al., 1993 and Kang et al., 2006), Anseriformes (goose, duck) (Huang, Shi, Z. Liu, Y. Liu, & Li, 2008), and Columbiformes (dove) (Mantei, Ramakrishnan, Sharp, & Buntin, 2008). Although the existence of the same cGnRH-I peptide was unknown in passerine birds for a long time, the mRNA encoding cGnRH-I was recently identified in zebra finches (Ubuka & Bentley, 2009; Stevenson, Lynch, Lamba, Ball, & Bernard, 2009) and in European starlings (Ubuka, Cadigan, Wang, Liu, & Bentley, 2009; Stevenson et al., 2009). The expression of cGnRH-I peptide in songbirds also has been suggested from its high-performance liquid chromatography (HPLC) elution pattern and its cross-reactivity with various GnRH antisera (Sherwood, Wingfield, Ball, & Dufty, 1988). Accordingly, cGnRH-I could be called avian GnRH-I (aGnRH-I) and we will use this naming in this chapter. There is a second form of GnRH, which is called chicken GnRH-II (cGnRH-II). Chicken GnRH-II was first found in chickens and subsequently in mammals (Miyamoto et al., 1984; King, Mehl, Tyndale-Biscoe, Hinds, & Millar, 1989; Morgan and Millar, 2004 and Millar, 2005) and eventually in all vertebrate groups (Norris, 2007; see also Volume 1, Chapter 2; Volume 2, Chapter 2; Volume 5, Chapter 2). The structure of cGnRH-II (pEHWSHGWYPG-NH 2) differs by three amino acids from mGnRH-I or aGnRH-I at positions five, seven, and eight. We will also refer to cGnRH-II as avian GnRH-II (aGnRH-II) to be consistent with the naming of aGnRH-I. Note that aGnRH-I and -II were formerly named cGnRH-I and -II, respectively.

Specific antibodies against avian GnRH peptides (aGnRH-I and aGnRH-II) have been made, and the histological localization of aGnRHs has been studied in the chicken and quail (Mikami et al., 1988 and Van Gils et al., 1993). In mammals, the GnRH-I neurons originate at the olfactory placode and migrate to preoptic-septal nuclei during embryonic development (Wray et al., 1989 and Schwanzel-Fukuda and Pfaff, 1989). The migration of aGnRH-I neurons from the olfactory placode to the forebrain along the olfactory nerve also has been observed in chickens (Norgren and Lehman, 1991, Akutsu et al., 1992 and Yamamoto et al., 1996). In adult birds, aGnRH-I-immunoreactive (-ir) cell bodies are found in a fairly wide area covering the hypothalamic preoptic area (POA) to the thalamic region. On the other hand, magnocellular aGnRH-II-ir cell bodies were found in the area dorsomedial to the nervus oculomotorius in the midbrain. Fibers immunoreactive for aGnRH-I or aGnRH-II were widely distributed in the telencephalon, diencephalon, and mesencephalon (midbrain). In sharp contrast to the existence of abundant aGnRH-I-ir fibers in the external layer of the ME, aGnRH-II-ir fibers were absent or less prominent in this area, suggesting that the major GnRH controlling pituitary function is aGnRH-I (Mikami et al., 1988 and Van Gils et al., 1993).

Specific radioimmunoassays (RIAs) for chicken LH (Follett, Scanes, & Cunningham, 1972), turkey LH (Burke, Licht, Papkoff, & Bona-Gallo, 1979), and chicken FSH (Scanes et al., 1977 and Sakai and Ishii, 1980) have been developed and used to measure the effect of GnRH on GTH release. The action of aGnRH-I on LH release from chicken anterior pituitary cells was first shown in vitro (Millar & King, 1983). Subsequently, the activities of aGnRH-I on LH and FSH release was shown both in vivo and in vitro in quail (Hattori et al., 1985). The activity of aGnRH-I on LH release was more marked than that on FSH release both in vivo and in vitro (Hattori et al., 1985). The activity of aGnRH-II (Miyamoto et al., 1984) on LH and FSH release was also shown in vivo and in vitro (Hattori, Ishii, & Wada, 1986). The activity of aGnRH-II on LH and FSH release was almost equal to that of aGnRH-I. Again, the activity of aGnRH-II on LH release was more marked than on FSH release both in vivo and in vitro. No synergism was observed between aGnRH-I and aGnRH-II on LH or FSH release in vitro (Hattori et al., 1986).

The physiological roles of aGnRH-I and aGnRH-II on LH release also have been investigated in chickens (Sharp et al., 1990). Egg laying of somatically mature hens is regulated by strain differences and environmental conditions. As ovulation is controlled by the preovulatory LH surge (as described in Section 4.1), the activity of GnRH may be higher in laying hens. The amount of aGnRH-I in the ME was higher in laying than in out-of-lay hens, as measured by RIA. Avian GnRH-II was not detected in the ME. The amount of aGnRH-I in the hypothalamus increased in cockerels at the onset of puberty, but the amount of aGnRH-II did not change. Active immunization of laying hens against aGnRH-I but not against aGnRH-II resulted in the complete regression of the reproductive system. Accordingly, it was concluded that GTH secretion in chickens is more likely to be controlled by aGnRH-I (Sharp et al., 1990). On the other hand, aGnRH-II may be involved in the control of sexual behaviors in various animals (Millar, 2003). Indeed aGnRH-II, but not aGnRH-I, administered to the brain increased copulation solicitation display, a female courtship behavior, in female white-crowned sparrows (Maney, Richardson, & Wingfield, 1997).

Three GnRH receptor (GnRH-R) subtypes (types I, II, and III) have been identified, each with distinct distributions and functions in vertebrates (Millar et al., 2004). These receptor subtypes belong to the G-protein-coupled receptor (GPCR) superfamily. Two receptor subtypes have been identified in chickens: type I (GnRH-R-I) (Sun et al., 2001a; 2001b) and type III (GnRH-R-III) (Shimizu & Bédécarrats, 2006), according to the classification by Millar et al. (2004). GnRH-R-I is widely expressed, and aGnRH-II has a higher binding affinity to this receptor and is more potent in stimulating accumulation of inositol trisphosphate, a secondary messenger molecule that can induce GTH release, than aGnRH-I (Sun et al., 2001a; 2001b). Inositol trisphosphate accumulation in response to aGnRH-II binding to GnRH-R-III was also more marked than in response to aGnRH-I. As fully processed GnRH-R-III mRNA was exclusively expressed in the pituitary, and its mRNA level was positively correlated with reproductive states in both sexes, it is likely that GnRH-R-III plays a role in the regulation of GTH secretion by pituitary gonadotropes (Shimizu & Bédécarrats, 2006). Despite the implication here that aGnRH-II is more effective in regulation of gonadotrope function, the current opinion is that aGnRH-I, and not aGnRH-II, is the dominant regulator of GTH release.

3.2. Gonadotropin-inhibiting Hormone (GnIH)

A hypothalamic neuropeptide, GnIH, has been found to be an inhibiting factor for LH release from the quail anterior pituitary (Tsutsui et al., 2000). Gonadotropin-inhibiting hormone-ir neuronal cell bodies are located in the paraventricular nucleus (PVN) in quail (Ubuka et al., 2003 and Ukena et al., 2003). These neurons project to the ME, thus providing a functional anatomical infrastructure that regulates anterior pituitary function. A cDNA encoding the GnIH precursor polypeptide has been cloned from the brains of quail (Satake et al., 2001), white-crowned sparrows (Osugi et al., 2004), European starlings (Ubuka et al., 2008a), and zebra finches (Tobari et al., 2010). The expression of GnIH precursor mRNA also has been observed in the PVN of these birds.

Gonadotropin-inhibiting hormone homologs are present in the brains of other vertebrates, such as mammals, amphibians, and fishes (Tsutsui and Ukena, 2006 and Fukusumi et al., 2006). These peptides, categorized as RFamide-related peptides (RFRPs), possess a characteristic LPXRF-amide (X = L or Q) motif at their C-termini in all vertebrates tested. Three LPXRF-amide (X = L or Q) peptide sequences are encoded in the GnIH precursor polypeptide, designated GnIH-related peptide-1 (GnIH-RP-1), GnIH, and GnIH-RP-2. Quail GnIH (SIKPSAYLPLRF-amide), quail GnIH-RP-2 (SSIQSLLNLPQRF-amide), starling GnIH (SIKPFANLPLRF-amide), and zebra finch GnIH (SIKPFSNLPLRF-amide) have been identified as mature endogenous peptides by mass spectrometric analyses (Satake et al., 2001, Ubuka et al., 2008a and Tobari et al., 2010).

The receptor for quail GnIH has been identified and its binding activities have been investigated (Yin, Ukena, Ubuka, & Tsutsui, 2005). Structural analysis of the quail GnIH receptor revealed that it belongs to the GPCR superfamily. A crude membrane fraction of COS-7 cells transfected with the quail GnIH receptor cDNA specifically bound GnIH, GnIH-RP-1, and GnIH-RP-2 in a concentration-dependent manner. The identified quail GnIH receptor mRNA was expressed in the pituitary as well as in various parts of the brain. The mammalian homolog of GnIH receptor is GPR147 (OT7T022, NPFF-1), and the mechanism of RFRP action on mammalian cellular events has been investigated (Fukusumi et al., 2006). RFamide-related peptides suppressed the production of cyclic-3’,5’-adenosine monophosphate (cAMP) in Chinese hamster ovarian cells transfected with GPR147, suggesting that the receptor couples to the α-subunit of the inhibitory G-protein (G αi). GPR147 mRNA is also expressed in various parts of the mammalian brain as well as in the pituitary, suggesting that there are multiple actions of GnIH within the central nervous system (Hinuma et al., 2000).

The actual release of GnIH into the hypothalamus–hypophysial portal system has not been reported in any vertebrate. However, the dense population of GnIH-ir fibers in the ME in quail (Tsutsui et al., 2000, Ubuka et al., 2003 and Ukena et al., 2003), house sparrows and song sparrows (Bentley, Perfito, Ukena, Tsutsui, & Wingfield, 2003), and European starlings (Ubuka et al., 2008a) suggests a role for GnIH in the regulation of pituitary function, at least in these birds. The same is true for white-crowned sparrows. The fact that GnIH inhibits release of GTHs from cultured quail and chicken anterior pituitary provides strong support for this function (Tsutsui et al., 2000 and Ciccone et al., 2004). Gonadotropin-inhibitory hormone administration to cultured chicken anterior pituitary inhibits not only the release of GTHs but also the synthesis of GTH subunit mRNAs (Ciccone et al., 2004). Nevertheless, direct regulation of pituitary function by GnIH may be regulated in a different way in some bird species either developmentally or temporally because there is no apparent GnIH-ir material in the ME in adult male Rufous-winged sparrows (Small et al., 2008), although GnIH receptor is expressed in the pituitary gland in this species (McGuire, Ubuka, Perfito, & Bentley, 2009). In other words, GnIH may directly inhibit pituitary function only during certain periods before sexual maturation or in response to stress, as described in Section 7.

To clarify the functional significance of GnIH in the control of avian reproduction, Ubuka, Ukena, Sharp, Bentley, and Tsutsui (2006) investigated the action of GnIH on the hypothalamic–pituitary–gonadal (HPG) axis in male quail. It is generally accepted that in avian species LH stimulates the formation of testosterone (T) by Leydig cells. Follicle-stimulating hormone and T stimulate growth, differentiation, and spermatogenetic activity of the testis (Follett, 1984 and Johnson, 1986). Luteinizing hormone is a protein complex, which is made of GTH common α and LHβ subunits, whereas FSH is a complex of GTH common α and FSHβ subunits. Peripheral administration of GnIH to mature quail via osmotic pumps for two weeks decreased the expression of GTH common α and LHβ subunit mRNAs in the pituitary. Concentrations of plasma LH and T were also decreased dose-dependently. Further, administration of GnIH to mature birds induced testicular apoptosis and decreased spermatogenetic activity in the testis. In immature birds, daily administration of GnIH for two weeks suppressed testicular growth and the rise in the concentration of plasma T. An inhibition of molt by juveniles also occurred after GnIH administration. These results show that GnIH may inhibit gonadal development and maintenance and also sexual development of birds by decreasing the synthesis and release of GTHs (Ubuka et al., 2006).

Although a dense population of GnIH neuronal cell bodies was found only in the PVN, GnIH-ir fibers were widely distributed in the diencephalic and mesencephalic regions in the Japanese quail (Ukena et al., 2003). Thus, it was hypothesized that GnIH may participate not only in the regulation of pituitary function, but also in behavioral and autonomic mechanisms. Immunohistochemical studies using light and confocal microscopy indicate that GnIH-ir axon terminals are in probable contact with aGnRH-I neurons in birds (Bentley et al., 2003). Thus, there is potential for the direct regulation of aGnRH-I neurons by GnIH neurons. Recently, Ubuka et al. (2008a) investigated the interaction of GnIH and aGnRH-I neurons in the European starling brain. Double-label immunocytochemistry showed GnIH axon terminals on aGnRH-I and aGnRH-II neurons (Bentley et al., 2003 and Ubuka et al., 2008a). Further, in-situ hybridization of European starling GnIH receptor mRNA combined with immunocytochemistry of aGnRHs showed the expression of GnIH receptor mRNA in both aGnRH-I and aGnRH-II neurons (Ubuka et al., 2008a). Central administration of GnIH inhibits the release of GTHs in white-crowned sparrows (Bentley et al., 2006a) in a manner similar to peripheral administration of GnIH (Osugi et al., 2004 and Ubuka et al., 2006). Accordingly, GnIH may inhibit the secretion of GTHs by decreasing aGnRH-I neuronal activity in addition to regulating the release of pituitary GTHs directly.

Central administration of GnIH also inhibits reproductive behavior of females in white-crowned sparrows (Bentley et al., 2006a). It is known that aGnRH-II enhances copulation solicitation in estrogen-primed female white-crowned sparrows exposed to male song (Maney et al., 1997b). As a result of the putative contact of GnIH neurons with aGnRH-II neurons in white-crowned sparrows (Bentley et al., 2003), Bentley et al. (2006a) investigated the effect of GnIH on copulation solicitation in females of this species. Centrally administered GnIH inhibited copulation solicitation in estrogen-primed female white-crowned sparrows exposed to the song of males without affecting locomotor activity. The result suggests that GnIH inhibits reproductive physiology and behavior not only by inhibiting the secretion of GTHs from the pituitary but also by directly inhibiting aGnRH-I and -II neuronal activity within the brain (Ubuka, McGuire, Calisi, Perfito, & Bentley, 2008).

Many hormones that are classified as neuropeptides are synthesized in vertebrate gonads in addition to the brain. Recently, GnIH and its receptor were found to be expressed in the gonads and accessory reproductive organs in Passeriformes and Galliformes (Bentley et al., 2008). Immunocytochemistry detected GnIH peptide in ovarian thecal and granulosa cells, testicular interstitial cells and germ cells, and pseudostratified columnar epithelial cells in the epididymis. Binding sites for GnIH were initially identified using in-vivo and in-vitro receptor fluorography, and were localized in ovarian granulosa cells as well as in the interstitial layer and seminiferous tubules of the testis. In-situ hybridization of GnIH-R mRNA in testes produced a strong reaction product that was localized to the germ cells and interstitium. In the epididymis, the product was also localized in the pseudostratified columnar epithelial cells. Similar data have been gathered from chickens, and estradiol (E 2) and/or progesterone (P 4) treatment of sexually immature chickens significantly decreased ovarian GnIH-R mRNA abundance (Maddineni, Ocón-Grove, Krzysik-Walker, Hendricks, Ramachandran, 2008). Further, GnIH decreased LH-induced T release from cultured dispersed testis (McGuire et al., 2009). The distributions and action of GnIH and its receptor suggest a role for GnIH in autocrine/paracrine regulation of gonadal steroid production and possibly germ cell differentiation and maturation in birds.

4. Mechanisms and Pathways Regulating Ovulation and Oviposition

4.1. Regulation of Ovulation

A hierarchy of developing follicles exists in the ovary of birds, and the largest follicle is ovulated at regular intervals. Many birds normally lay one egg each day during the breeding season. They usually lay two to ten eggs (two to ten days) in a sequence (clutch), but the actual number varies greatly among species. Between the clutches there are one or more pause days. Generally clutch size is smaller and the interval between eggs is longer in species producing large eggs. Many birds lay a fixed number of eggs in a clutch (determinate layers), but others can continue laying for long periods (indeterminate layers) (Follett, 1984). Clutch size also tends to increase with latitude (Ricklefs, 1970).

In domestic chickens, ovulation occurs six to eight hours after the preovulatory LH surge and the egg spends about 24 hours in the oviduct before it is laid. The next ovulation occurs 15 to 75 minutes after the oviposition, except after the last oviposition in a clutch. As a result of this temporal relationship, the time of oviposition is a practical index of the time of ovulation. Under light–dark cycles of 14L : 10D, chickens usually lay their eggs in the first half of the photophase whereas quail lay late in the day and early in the night. In both cases, the preovulatory surge of LH occurs six hours plus one day before the egg is laid. Under continuous light, the oviposition rhythms are free-running, and egg laying occurs throughout the 24 hours (Warren and Scott, 1936, Morris, 1961 and Wilson and Cunningham, 1981). Normally, the light–dark cycle entrains the rhythm, with dusk being the primary cue in chickens (Bhatti & Morris, 1978a; 1978b) and dawn in Japanese quail (Tanabe, 1977). Other factors such as feeding, temperature changes, and bright/dim light are capable of entrainment when hens are illuminated constantly (Morris & Bhatti, 1978).

Ovulation depends on a surge of LH four to eight hours earlier, as determined by studies employing injection of LH or GnRH in intact birds or hypophysectomy (Fraps, 1970 and Van Tienhoven and Schally, 1972). A surge in plasma LH occurs four to eight hours before ovulation in chickens (Wilson and Sharp, 1973 and Etches and Cunningham, 1977), turkeys (Mashaly, Birrenkott, El-Begearmi, & Wentworth, 1976), and quail (Tanabe, 1977), and presumably other species. A constant relationship of about 30 hours exists between the peak of LH and the resulting oviposition, and the LH peak is absent on the last day of a sequence. Plasma FSH shows only minor changes during the ovulatory cycle (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, 1976).

As P 4, but not estrogens, can induce premature ovulation in the hen, Fraps (1955; 1970) proposed that P 4 triggers the preovulatory LH surge by a positive feedback mechanism. A single major peak of P 4 coincides with that of LH (Furr et al., 1973, Senior and Cunningham, 1974 and Etches and Cunningham, 1977). This peak is delayed by two to three hours each day in a laying sequence and is absent when no ovulation takes place. A preovulatory peak of E 2 occurs with that of LH but ovulation can take place in its absence (Laguë, Van Tienhoven, & Cunningham, 1975). The effects of various steroids on the LH surge and ovulation have been tested. Progesterone almost always triggers an LH surge that begins 15 to 45 minutes after intramuscular injection, peaks within two hours, and lasts for about six hours. Gonadotropin-releasing hormone seems to relay the effect of P 4 on the LH surge, because anti-GnRH antibody administration blocks the effect of P 4 (Fraser & Sharp, 1978). Intrahypothalamic injections of P 4 also trigger ovulation (Ralph & Fraps, 1960). In summary, the P 4 surge appears to be important for initiating ovulation.

The ovulated egg is captured by the ostium of the oviduct. Fertilization and deposition of the first layer of albumen occur here. The ovum passes down the oviduct through highly differentiated regions that have specific functions. Further albumen is laid down in the magnum, and membranes surround the developing egg in the isthmus. On reaching the shell gland (also known as the uterus), a shell and pigment are deposited (Solomon, 1983). Finally, oviposition occurs through the vagina and cloaca. Note that since there is only one ovary and one oviduct, further ovulations cannot occur unless oviposition has occurred (Sharp, 1980).

4.2. Regulation of Oviposition

Oviposition means expulsion of the egg from the oviduct to the external environment and is a common phenomenon in vertebrates other than eutherian mammals. Avian oviposition is thought to be regulated by a neurohypophysial hormone, AVT, together with ovarian hormones and prostaglandins (PGs) through the induction of uterine contractions (Munsick, Sawyar, & Van Dyke, 1960; Rzasa and Ewy, 1970, Hertelendy, 1972, Wechsung and Houvenaghel, 1976, Olson et al., 1978, Toth et al., 1979 and Takahashi et al., 1992). Regulation of oviposition by the sympathetic nervous system using galanin as a neurotransmitter seems to exist in quail (Li, Tsutsui, Muneoka, Minakata, & Nomoto, 1996; Tsutsui, Azumaya, Muneoka, Minakata, & Nomoto, 1997; Tsutsui et al., 1998 and Sakamoto et al., 2000). The expression of galanin in the sympathetic ganglia is regulated by ovarian sex steroids (Ubuka, Sakamoto, Li, Ukena, & Tsutsui, 2001).

The neurohypophysial hormones AVT and MST represent the nonmammalian homologs to arginine vasopressin and oxytocin, respectively (Acher, Chauvet, & Chauvet, 1970). However, in birds, the oxytocic effect of AVT is greater than that of MST (Saito and Koike, 1992 and Barth et al., 1997). Plasma AVT increases sharply at the time of oviposition to induce uterine contraction (Nouwen et al., 1984, Tanaka et al., 1984 and Shimada et al., 1986) and decreases within 30 minutes of an egg being laid (Koike, Shimada, & Cornett, 1988). Elevation of plasma AVT at the time of oviposition is accompanied by a depletion of AVT concentration in the neurohypophysis (Sasaki, Shimada, & Saito, 1998).

Magnocellular neurons producing AVT are found in the preoptic nucleus, the supraoptic nucleus, and the PVN of the hypothalamus. A sexually dimorphic population of parvocellular AVT neurons is observed from the mediocaudal part of the preoptic region to the dorsolateral part of the bed nucleus of stria terminalis in male birds, suggesting a role in the control of male sexual behaviors (Jurkevich & Grossmann, 2003). Effects of AVT on various male reproductive behaviors, such as aggressive and courtship behaviors, including song production, have been documented (Kihlström & Danninge, 1972; Maney, Goode, & Wingfield, 1997; Castagna et al., 1998 and Goodson, 1998a; 1998b; Goodson & Adkins-Regan, 1999). There is also a role for AVT, along with corticotropin-releasing hormone (CRH), in ACTH release from the anterior pituitary (Castro et al., 1986, Romero et al., 1998 and Madison et al., 2008).

5. Mechanisms and Pathways Regulating Prolactin (PRL) Secretion

A period of egg incubation occurs in the vast majority of birds (Drent, 1975). Brood patches develop in virtually all birds and seem to be used to transfer body heat to the eggs. The changes in the brood pouch skin are substantial, involving hyperplasia of the epidermis, an edema leading to wrinkling of the skin, and extra vascularization. The whole process is thought to be controlled by a synergism between PRL and the sex steroids (Jones, 1971 and Drent, 1975). Estrogens and P 4 are the active agents in the female, but where males incubate these are replaced by androgens.

Injections of PRL induce chickens to incubate eggs (Riddle et al., 1935 and Sharp et al., 1988), and maintain readiness of ring doves to incubate their clutches (Lehrman and Brody, 1964 and Janik and Buntin, 1985). In species that hatch precocial young, PRL levels rise slightly during egg-laying, but then increase markedly throughout incubation and fall immediately when the chicks have hatched. In female birds that fail to incubate, as well as in males, PRL never rises above baseline concentrations (mallards (Goldsmith & Williams, 1980)). In species that produce altricial young, PRL is also very high during incubation but it often stays high whilst the young are fed in the nest (canary (Goldsmith, 1982)). In ring doves and other Columbiformes, PRL causes growth of the crop gland and production of crop milk for feeding of young for the first few days after hatch. In these birds, plasma levels of PRL do not rise during egg-laying and the 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 female turkeys the action of PRL on incubation behavior is facilitated by the combined action of E 2 and P 4 (El Halawani, Silsby, Behnke, & Fehrer, 1986).

In birds, PRL secretion is actively stimulated by release of VIP from the ME. Mammalian VIP specifically stimulated PRL release in vivo and in vitro in bantam hens (Macnamee, Sharp, Lea, Sterling, & Harvey, 1986) and turkeys (Opel and Proudman, 1988 and Proudman and Opel, 1988), while immunohistochemical studies showed the presence of VIP-ir nerve terminals in the ME in quail (Yamada, Mikami, & Yanaihara, 1982), bantam hens (Macnamee et al., 1986), and pigeons (Péczely & Kiss, 1988). The structure of hypothalamic chicken and turkey VIP is regarded as the same as that isolated from the chicken gut, which is a 28-amino-acid peptide differing from mammalian VIP in four amino acids (Nilsson, 1975). Both chicken and turkey VIP cDNAs have been sequenced (Talbot, Dunn, Wilson, Sang, & Sharp, 1995; You, Silsby, Farris, Foster, & El Halawani, 1995). Immunization against VIP inhibits PRL secretion in bantam hens (Sharp, Sterling, Talbot, & Huskisson, 1989) and turkeys (El Halawani, Pitts, Sun, Silsby, & Sivanandan, 1996). Daily injections of anti-VIP caused incubating bantam hens to desert their nests. On the other hand, disruption of incubation behavior with anti-VIP was prevented by concomitant administration of ovine PRL (Sharp et al., 1989). The amount of VIP was significantly higher in the ME and cell bodies in the medial basal hypothalamus in incubating as compared to actively laying hens (Sharp et al., 1989). Vasoactive intestinal peptide mRNA and peptide levels were low in nonphotostimulated turkeys, higher in laying hens, and highest in incubating hens. Changes in VIP paralleled the changes in plasma PRL levels (Chaiseha, Tong, Youngren, & El Halawani, 1998). Dopaminergic control of PRL secretion also has been suggested in turkeys (Youngren, Pitts, Phillips, & El Halawani, 1996; Youngren, Chaiseha, & El Halawani, 1998).

The peak in PRL concentrations coincides with a decrease in LH concentrations and coincident gonadal regression in many bird species (Sharp & Sreekumar, 2001), which suggests a role for PRL in the termination of breeding. However, this is unlikely because administration of exogenous PRL does not on its own cause the onset of photorefractoriness (Goldsmith, 1985). Further, active immunization of starlings against VIP completely blocks PRL secretion but does not prevent gonadal regression (Dawson & Sharp, 1998). The timing of high levels of PRL is also closely linked to molt, premigratory fattening, and migration (Meier and MacGregor, 1972, Meier, 1972 and Dawson and Goldsmith, 1983).

6. Mechanisms and Pathways Regulating Seasonal Reproduction

6.1. Seasonal Reproduction in Birds

Birds have presumably evolved the timing of their breeding so that they can maximize the production of offspring, and laying is normally timed so that young are in the nest when there is enough food for them to be raised (Lack, 1968). Baker (1938) suggested that seasonal breeding is controlled by two sets of environment factors: ‘ultimate’ and ‘proximate’ factors. The most important ultimate factor for birds is the availability of an adequate food supply for the hatchlings as well as for the mother during the final stages of ovarian development. Other ultimate factors operating in special situations are competition, nesting conditions, predation pressure, and climate factors. However, these ultimate factors are often not those that trigger and regulate the secretion of reproductive hormones, because it is necessary to anticipate the hatching date and to begin preparations for breeding some weeks or months ahead of the time when young must be produced.

In birds living in mid and high latitudes, there is excellent experimental evidence that the annual change in day length controls the timing of breeding, and it may be assumed that photoperiod is a proximate factor for birds living in such regions (Follett, 1984). Other environmental factors are also used to accelerate or retard photoperiodically induced gonadal growth (Farner & Follett, 1979). These include the presence of males for stimulating ovarian development (Marshall, 1936, Hinde, 1965 and Cheng, 1979), ambient temperature (Perrins, 1973), and rainfall (Leopold, Erwin, Oh, & Browning, 1976). It is thought that photoperiod is not the proximate factor for many tropical and desert species (Marshall, 1970). Reproduction of tropical birds, such as African stonechats (Gwinner & Scheuerlein, 1999) and zebra finches (Bentley, Spar, MacDougall-Shackleton, Hahn, & Ball, 2000) can respond to changing photoperiod although the experimental length of the photoperiods used in these studies exceeded that of the tropics. However, studies on spotted antbirds suggest that tropical birds can respond to natural slight photoperiodic changes (Hau et al., 1998 and Beebe et al., 2005). The proximate factors used to time breeding in tropical birds remain largely unknown although correlative analyses suggest rainfall, territory, nest site availability, nest materials, and food supply as being involved (Immelmann, 1971 and Zann et al., 1995). Stonechats may respond to low light intensity as a predictive cue for rainfall (Gwinner & Scheuerlein, 1999). The reproductive axis of tropical birds may remain in a state of ‘readiness to breed,’ and full functionality may be triggered by the relevant proximate cues (Perfito et al., 2006 and Perfito et al., 2008). Although crossbills live in high latitudes, breeding can occur opportunistically at any time between January and August in response to their food supply. They feed on the seeds of coniferous trees, which are produced in different amounts in different years, and at unpredictable times of the year. However, they have a short, fixed nonbreeding period in fall when they appear to be photorefractory (Hahn, 1998).

The vast majority of temperate-zone passerines undergo dynamic seasonal changes in their reproductive activities. Gonadal development occurs in spring in response to increasing day length (photostimulation). However, the gonads are maintained in a functional condition only for a short period, and they spontaneously regress after extended exposure to long day lengths (absolute photorefractoriness). After becoming photorefractory, exposure to short day length is required to regain photosensitivity and thus allow for photostimulation (Wingfield & Farner, 1980). Photorefractoriness seems to have evolved to minimize the costs of reproducing in the rapidly deteriorating environmental conditions of fall and winter (Follett, 1984). The only well-studied birds that do not become photorefractory are some species of pigeon and dove (Murton & Westwood, 1977).

A condition similar to absolute photorefractoriness is relative photorefractoriness. The main difference is that, once relative photorefractoriness has been induced and the gonads have regressed, a subsequent substantial increase in day length will once more initiate reproductive maturation—without the need for a short-day-length ‘sensitization,’ or photosensitive, stage (Robinson & Follett, 1982). For example, if Japanese quail experience day lengths of over 11.5 hours, rapid gonadal development occurs. After about three months, and when (in the wild) day length decreases below 14.5 hours, complete gonadal regression occurs—in a similar manner to absolute photorefractoriness (Nicholls, Goldsmith, & Dawson, 1988). However, if the day length is subsequently artificially increased further, a full return to reproductive maturity occurs. Indeed, if quail are maintained on any constant long day length, no form of photorefractoriness will be elicited unless they experience a decrease in day length, e.g., from 23 to 16 hours (Nicholls et al., 1988). This suggests a shift in the critical day length in birds that are relatively photorefractory—a shift that appears to depend on the photoperiodic history of such birds (Robinson & Follett, 1982). There does not seem to be any change in critical day length in birds that exhibit absolute photorefractoriness, regardless of their photoperiodic history (Dawson, 1987).

Song sparrows and house sparrows show characteristics of both absolute and relative photorefractoriness (Dawson, King, Bentley, & Ball, 2001). Song sparrows (Wingfield, 1983) and house sparrows (Dawson, 1998a) eventually become photorefractory during exposure to long photoperiods, but the timing can vary widely among individuals. If the photophase is decreased slightly, gonadal regression occurs sooner and is more synchronized among individuals. Moreover, song sparrows can show renewed gonadal maturation before exposure to short photoperiods (Wingfield, 1993).

Seasonal changes in reproductive activities are correlated with GTH secretion. The primary effect of long day lengths on stimulating GTH secretion has been shown in quail (Follett, 1976), white-crowned sparrows (Wingfield & Farner, 1980), tree sparrows (Wilson & Follett, 1974), canaries (Nicholls, 1974), ducks (Balthazart, Hendrick, & Deviche, 1977), starlings (Dawson & Goldsmith, 1983), and many other birds. If male quail are transferred from short day lengths (8L : 16D) to long day lengths (20L : 4D), the levels of FSH and LH rise substantially during the first week of photostimulation. Testicular growth and steroidogenesis begin and maturity is reached in about five weeks (Follett & Robinson, 1980). Gonadal steroids affect GTH secretion by negative feedback (King et al., 1989a and Dunn and Sharp, 1999). Gonadal steroids also induce sexual behavior, development of secondary sexual characteristics, and spermatogenesis (Follett & Robinson, 1980). Female quail also grow their ovaries as a result of increased GTH secretion induced by long day lengths (20L : 4D). Gonadotropin levels becomes basal after transferring quail from long days to short days (8L : 16D) (Gibson, Follett, & Gledhill, 1975). On the other hand, in most of the temperate-zone passerine birds, which undergo spontaneous photorefractoriness after exposure to long days, GTH secretion is diminished and gonadal collapse occurs after a species-specific number of long days (Follett, 1984).

Seasonality continues in the absence of the gonads. Castrated or intact quail show an identical time-course in LH and FSH secretion under natural photoperiods over two consecutive years, the difference being that in summer the GTH levels in castrated birds are higher, as a result of lack of negative feedback from gonadal steroids (Follett, 1984). A similar annual cycle of LH secretion has been observed in the plasma of intact and castrated white-crowned sparrows (Mattocks, Farner, & Follett, 1976). It is also thought that gonads are not required for photorefractoriness to develop, because castrated white-crowned sparrows (Wingfield, Follett, Matt, & Farner, 1980), canaries (Storey, Nicholls, & Follett, 1980), and starlings (Dawson & Goldsmith, 1984) show a spontaneous fall in GTH level under long days. Castration of photorefractory canaries does not cause enhanced LH secretion, but when photosensitivity is regained under short days there is an immediate rise in plasma LH (Nicholls & Storey, 1976).

Birds seem to measure daylength using their circadian clock. In a classic experiment, white-crowned sparrows held on short day lengths (8L : 16D) were placed in continuous darkness. When birds were exposed to a single eight-hour photophase, an increase in LH occurred only if the photophase coincided with a time period 12–20 hours after the subjective dawn, as judged by the circadian rhythms of the birds (Follett, Mattocks, & Farner, 1974). These data imply that a circadian rhythm of sensitivity to light, or photoinducibility, exists in the photoperiodic time measurement system of these birds. There are two possible models of how circadian rhythms might be involved in photoperiodic time measurement in birds (Goldman, 2001). The ‘external coincidence model’ assumes the organism possesses a circadian rhythm of ‘photosensitivity’. If coincidence between this rhythm and light occurs under long days, it induces GTH secretion. The ‘internal coincidence model’ assumes the induction to occur when coincidence is established between two separate circadian oscillators (usually dawn and dusk oscillators). As a consequence of using a circadian clock for photoperiodic time measurement, light is not required throughout the day to induce gonadal growth, but pulses of light simulating dawn and dusk can cause induction if one of the pulses coincides with the phase of photosensitivity (Follett, 1973). As with white-crowned sparrows, when 15-minute pulses of light were given at different times in the night to quail on the basic photoperiod of 6L : 18D, induction occurred only if the pulses were within 12 to 16 hours of dawn (Follett & Sharp, 1969).

Light intensity can also modify the reproductive responses of birds under the same photoperiod (Bissonnette, 1931; Bartholomew, 1949). In the experiment conducted by Bentley, Goldsmith, Dawson, Briggs, and Pemberton (1998), photosensitive starlings transferred from short days to long days of different light intensities underwent graded reproductive responses according to the light intensities they experienced. Interestingly, the responses observed, such as the growth in their testes size and the development of photorefractoriness, were similar to those seen in starlings exposed to different photoperiods. At face value, these data contradict the external coincidence model in that light falling in the photoinducible phase should cause a long-day response. However, this discrepancy might be explained by the possibility that low light intensities only weakly entrain the circadian oscillations of the photoinducible phase, so that light is experienced in only part of the photoinducible phase.

6.2. Seasonal Changes in Gonadotropin-releasing Hormone (GnRH)

Radioimmunoassay and immunocytochemistry (ICC) using GnRH antisera have numerous times demonstrated cyclic changes in GnRH in songbirds in response to changing photoperiod. Radioimmunoassay revealed that hypothalamic GnRH content did not increase significantly during the first six weeks of photostimulation in