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Publications from USDA-ARS / UNL Faculty U.S. Department of Agriculture: AgriculturalResearch Service, Lincoln, Nebraska

1995

Endocrinology of the Avian Reproductive SystemMary Ann OttingerUniversity of Maryland - College Park

Murray R. BakstUnited States Department of Agriculture

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Ottinger, Mary Ann and Bakst, Murray R., "Endocrinology of the Avian Reproductive System" (1995). Publications from USDA-ARS /UNL Faculty. 622.http://digitalcommons.unl.edu/usdaarsfacpub/622

Journal of Avian Medicine and Surgery 9(4):242-250, 1995 C 1995 by the Association of Avian Veterinarians

Review Article

Endocrinology of the Avian Reproductive System Mary Ann Ottinger, PhD, and Murray R. Bakst, PhD

Abstract: The purpose of this review is to provide an overview of the avian reproductive system. Attention is given to the neuroendocrine regulation of hypothalamic and pituitary gland hormones as well as the target tissues regulated by these hormones. Emphasis is placed on the dynamics of the system and the effects of alterations resulting from environmental and other influences on the function of the reproductive system. The ovulatory cycle, oviduct, and shell gland are discussed relative to egg formation and the hormonal regulation of this process. Testicular function and the cellular bases for spermatogenesis and steroid production are also discussed.

Key words: reproductive biology, endocrine system, accessory sex structures, birds

Introduction

Avian species utilize a variety of reproductive strategies that allow them to reproduce under a diversity of conditions and environments. Endo- crine and behavioral components of reproduction are directed by the hypothalamus in response to environmental triggers, such as photoperiod. Su- perimposed on these triggers are internal factors such as stage of the life cycle and general health.

The primary components of the "integrated" reproductive system are the hypothalamus, pitui- tary gland, and gonads. Accessory organs, which include the oviduct, excurrent duct system, and associated cloacal structures, are also critical to reproductive success. Moreover, endocrine and behavioral components of reproduction must function synchronously for successful reproduc- tion.

The purpose of this review is to provide an overview of the male and female reproductive en- docrine system in birds. This includes neuroen- docrine regulation of hypothalamic and pituitary gland hormones, gonadal function, and reproduc- tive tract function. Emphasis is placed on the dy- namics of the system and subsequent effects on the function of the gonads and the accessory sex

organs. The ovulatory cycle relative to the oviduct and its functions is also reviewed.

Neuroendocrine Regulation of Hypothalamic Processes and

Behavioral Responses

As in other vertebrates, the male and female avian reproductive systems are regulated by the hypothal- amus-pituitary-gonadal axis (Fig. 1). The hypothal- amus produces a gonadotropin-releasing hormone (GnRH) that stimulates pituitary gland production of luteinizing hormone (LH) and follicle-stimulating hormone (FSH), which in turn regulate ovarian and testicular function. Gonadal steroids, primarily tes- tosterone, estradiol, and progesterone return to the central nervous system through the bloodstream and provide a feedback regulation of hypothalamic GnRH production and release. Some additional in- ternal and external factors regulate and modulate hy- pothalamic function. In this section, we review the regulation of GnRH in avian species, particularly in reference to regulation of the system in the breeding adult.

Gonadotropin-releasing hormone (GnRH)

In contrast to mammalian GnRH, two chemical forms of avian GnRH are known to exist: chicken GnRH-I (cGnRH-I) and chicken GnRH-II (cGnRH- 1).1,2 Since the discovery of these hormones several years ago, some avian species have been shown to have both cGnRH-I and cGnRH-II.3,4 Moreover, other forms of GnRH have been discovered in other

From the Department of Poultry Science, University of Mary- land, College Park, MD 20742, USA (Ottinger), and the Germ- plasm and Gamete Physiology Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD 20705, USA (Bakst).

242

OTINGER AND BAKST-AVIAN REPRODUCTIVE ENDOCRINOLOGY 243

* Hypothalamus: neuropeptides and neurotransmitters regulate the synthesis and release of cGnRH-I. Potential regulatory peptides include VIP, Neuropeptide Y, Substance P, and the opioid peptides. In addition, the monamines have been implicated in regulation of cGnRH-I.

* Pituitary Gland: Alpha and beta subunits are synthesized to produce the gonadotropins, LH and FSH. Production of the mRNA for these hormones is regulated by GnRH and further modulated by gonadal steroids.

* The gonads produce steroids which feed back to the hyothalamus to regulate cGnRH-l production and sexual behavior. The accessory and secondary sex structures are also dependent on steroid hormone support for their morphology and function.

Hypothraatrus cGnRHCI

Pituitary Gland LH

FSH

Gonads/Gamete Production Testosterone

Estradiol/Progesterone

Accessory/Secondary Sex Structures Oviducts/Vas deferens Comb/Wattleslother characteristics

Figure 1. A schematic diagram of the avian hypothalamic-pituitary-gonadal (HPG) axis, illustrating the neuroendo- crine regulation of hypothalamic and pituitary gland hormones, and their effect on reproductive organs.

species and phyla. Evidence points to the cGnRH- II peptide as one that is very old phylogenetically.5-8 In spite of the presence of cGnRH-II across many species and phyla, including mammals, its function is unclear in most of the species in which it has been observed. Notwithstanding, there is evidence for separate roles of different forms of GnRH that occur in the central nervous system. Specifically, there are convincing data in fish that cGnRH-II plays a role in the regulation of courtship and mat- ing behavior, with little role in the regulation of pi- tuitary gland gonadotropins.9,10 A role for GnRH as a modulator of reproductive behavior has been hy- pothesized in some mammals, including voles.11 Their experiments provided convincing evidence for the stimulation of male sexual behavior in cas- trated males given low levels of exogenous testos- terone. We found similar effects in male quail. Cas- trated male quail given testosterone implants that provide insufficient testosterone to stimulate sexual behavior will show mating behavior for a short pe- riod of time in response to GnRH injection (Cortes- Burgos and Ottinger, unpubl. data). Additional in- triguing data have been collected by Cheng and col- leagues,12,13 which showed that the GnRH system is responsive to social cues and interactions, thereby providing an additional level of environmental reg- ulation of the reproductive axis. Additional research is needed to clarify the potential role of GnRH as a neuromodulatory in avian sexual behavior.

Other experiments have been done to further our understanding of the functional relationship in reg- ulation of cGnRH-II as compared with cGnRH-I. Immunocytochemical localization of cGnRH-I and

cGnRH-II in chickens, turkeys, and quail show a general distribution of cGnRH-II throughout the brain and a primary concentration of cGnRH-I in the hypothalamus.4,14-~'6 Cell bodies containing c- GnRH-I-reactive material are located in the preoptic and septal areas of the central nervous system, with most axonal projections terminating in the median eminence. Although one laboratory has reported cGnRH-II immunoreactivity near the median emi- nence, we were not able to measure cGnRH-II in assays of dissected median eminence punches.16,17 Additional information has been gained from in vitro studies of hypothalamic slices from adult male quail, in which there is substantial release of c- GnRH-I and little or no release of cGnRH-II.17 Stimulation of release by norepinephrine, which is known to stimulate GnRH release, resulted in re- lease of cGnRH-I but not cGnRH-II.

Regulation of the GnRH system in birds has been under study for many years, with recent studies making the distinction between cGnRH-I and c- GnRH-II (for review, see Ottinger'8). A variety of experimental approaches have been used, including manipulation of the system by pharmacologic agents or endocrine treatments, immunohistochem- ical localization of GnRH, and steroid or peptide receptor treatments. These studies have shown that catecholamines are located in areas involved in the regulation of the GnRH system and are likely to modulate the system during various stages of the life cycle.19-21 Furthermore, the cGnRH-I system ex- hibits age-related alterations as well as depressed function in refractory birds, which are birds that have become unresponsive to stimulatory photope-

244 JOURNAL OF AVIAN MEDICINE AND SURGERY

riods.22-26 Other peptides, including vasotocin, va- soactive intestinal peptide, neuropeptide Y, and opioid peptides have been implicated in the neu- roendocrine regulation of GnRH, often because neurons containing these peptides are in close ana- tomic proximity to cGnRH-I-containing neurons. These peptides have been implicated through ex- perimental effects on the reproductive system.27-31 Studies of neuroregulatory effects of these peptides provide evidence that opioid peptides inhibit the GnRH system, whereas the effects of vasotocin, va- soactive intestinal peptide, and neuropeptide Y are unclear. In summary, most evidence points to c- GnRH-I as the endogenous hypothalamic hormone critical for stimulating synthesis and release of pi- tuitary gland LH and FSH, and this GnRH action is mediated by calcium.14,32

As mentioned earlier, investigators have also used in vitro methods to further elucidate regulation of cGnRH-I release in birds. Early studies with hy- pothalamic explants showed that GnRH release is affected by sexual maturation.33-37 Further, these studies gave evidence for regulation of GnRH re- lease by norepinephrine and other peptides in vitro, presumably in a manner similar to their apparent roles in vivo. We also examined cGnRH-I release in vitro.38,39 However, our experiments differed from those previously conducted in two respects. First, cGnRH-I was specifically measured with a highly sensitive and specific enzyme immunoassay and second, our dissections produced longitudinal hy- pothalamic slices. This modification preserved many of the connections between the cell bodies in the preoptic and lateral septal regions with the ax- onal terminals in the median eminence.40 Subse- quent experiments with these modifications showed that challenge with regulatory peptides, including norepinephrine and epinephrine, were very potent in stimulating a large amplitude cGnRH-I release, but these neurochemicals did not affect the frequen- cy of episodic release.38 Further, these catechol- amines were found to act on the alpha and beta adrenergic receptor systems (Li et al., unpubl. data). Separate experiments demonstrated that exposure to gonadal steroids for several hours exerted an inhib- itory effect on cGnRH-I release, whereas short-term estradiol exposure stimulated cGnRH-I release in vitro.39 Conversely, opioid peptides, including met- enkephalin and B-endorphin, acted in a dose-depen- dent inhibitory manner and depressed both baseline and norepinephrine-stimulated cGnRH-I release with reduced amplitude of the episodic release.41,'42

To summarize, these studies provide additional insight into the regulation of cGnRH-I release in the sexually maturing and mature bird. The adrenergic

systems appear to be important in stimulation of cGnRH-I release, whereas opioid peptides appear to inhibit cGnRH-I release. These results provide ev- idence for some of the regulatory elements that are likely to be active in the avian hypothalamus. In- terestingly, assays of cGnRH-I and catecholamines show changes during the aging process.40 And fi- nally, epinephrine concentrations were highly mea- surable in "punches" of avian hypothalamic areas as compared with mammals in which epinephrine levels are extremely low in the central nervous sys- tem (Ottinger et al., unpubl. data). This implies that the avian system may use both norepinephrine and epinephrine as well as a number of other neuropep- tides to regulate cGnRH-I production and release.

Courtship and mating behavior

There is a large body of literature on the vast diversity of reproductive behavior in birds and the endocrine and neuroendocrine mechanisms that modulate these behaviors in avian species. Lehr- man's laboratory provided some of the first thor- ough studies of the linkages between hormones and behavior in birds. Their early studies43,44 provided detailed descriptions of the behavioral patterns in- volved in courtship, mating, incubation, and paren- tal care in the ring dove. Subsequent studies have built upon this foundation and have characterized the role of steroid hormones, prolactin, and neuro- peptides in these behaviors.11,45-50 Song birds have been studied extensively and are under investigation in many laboratories. These studies have provided evidence for sexually dimorphic neuroanatomic structures that are involved in endocrine and behav- ioral components of reproduction (for review, see Panzica et a129,30). Studies in the zebra finch have demonstrated that testosterone and its metabolites regulate sexual behavior, and that these responses are modulated by neuropeptide and monoamine neuroregulatory systems.51-53 A number of other species, including chickens, turkeys, and Japanese quail have also been investigated (for review, see Ottinger24). Studies in the turkey hen have shown that the neuropeptide vasoactive intestinal peptide is important in the regulation of prolactin, a hor- mone associated with broody behavior.28

The male bird will exhibit elaborate courtship and mating behaviors to which the female may or may not be receptive. Like its mammalian counter- part, testosterone is required for avian male sexual behavior and must be aromatized to its biologically active metabolite, estradiol, in target areas in the central nervous system.54',55 As in the regulation of the endocrine portion of the reproductive axis, sex-

OTTINGER AND BAKST-AVIAN REPRODUCTIVE ENDOCRINOLOGY 245

ual behavior is also modulated by neuropep- tides.30,51,56 Although the exact roles of many of these neuropeptides are unclear, investigations have focused on vasotocin, dopamine, norepinephrine, opioid peptides, and neuropeptide Y and their ef- fects on sexual behavior. The regulation of sexual behavior is further altered by the effects of social interactions, which can exert powerful effects on reproductive success and overall well-being of the individual.57"' In summary, many of the data on neu- roendocrine and peptide regulation of sexual behav- ior support the notion that endocrine and behavioral components of reproduction are modulated through these neuroendocrine systems.

Pituitary Gland Response and Gonadotropin Production

As previously discussed, gonadotropins produced by the pituitary gland are regulated primarily by GnRH. There is further modulation by gonadal ste- roids, which reach the gonadotrophs of the anterior pituitary gland to act in a weak negative feedback capacity. There is growing evidence that inhibin, which has been characterized in the female chicken, is produced in the ovary and acts to inhibit pituitary gonadotropin. Although cGnRH-II does not appear to reach the pituitary gland in birds, both forms of GnRH stimulate LH release in vitro.58 Several se- cretagogues have been found effective in releasing LH from dispersed pituitary gland cells.59 In addi- tion, gonadotropins occur as chemical isoforms.60 This is potentially important as a mechanism for more subtle regulation because of differing biolog- ical activity of the isoforms. At the molecular level, the LH molecule is composed of an alpha and beta subunit.61 Further, the alpha subunit is also common to FSH and thyroid-stimulating hormone. At least in mammals, the genetic expression of the alpha and beta subunits are modulated by a number of factors, including gonadal steroids and peptides.62

The Male System

Testicular morphology and excurrent duct system

The paired testes are located in the anterior aspect of the abdominal cavity just above the kidneys. Spermatogenesis takes place in the seminiferous tu- bules, which contain Sertoli and germ cells (Fig. 2). The Sertoli cells are responsive primarily to FSH and, as in mammals, produce inhibin. Spermatogen- esis has been recently reviewed elsewhere.63,64 Dis- persed between the seminiferous tubules are the an- drogen-producing cells--the Leydig cells. Once se-

creted, testosterone, which is the major androgen produced and secreted from the testes,65 is enzy- matically reduced to its active metabolite, 5-alpha dihydrotestosterone.65,66

Sperm are transported through a rudimentary ep- ididymal region into the ductus deferens and stored until ejaculation. Male birds do not possess acces- sory sex glands, which in mammals add fluid to the sperm. Alternatively, when Galliformes ejaculate the semen is mixed with a lymphlike transparent fluid.63,64 Nevertheless, galliform semen remains highly concentrated (about 6 billion and 10 billion sperm per milliliter in chicken and turkey semen, respectively). In the poultry industry, a semen ex- tender, which is a cell culture medium specifically designed for sperm, is used to dilute semen. In this way, far greater numbers of hens can be artificially inseminated on a per-male basis than if the semen was used undiluted. The extender also sustains sperm viability for several hours (for further infor- mation on artificial insemination technology includ- ing semen collection, dilution evaluation, liquid storage, and cryopreservation, see Bakst and Wis- hart67).

The Female System

The ovary of the reproductive female is remark- able in that the hen ovulates almost daily, with some commercial layer strains of chickens laying over 300 eggs per year. Other species, such as cranes, have a longer period of time between ovulation and oviposition, which reflects increased time that the egg spends in the reproductive tract, particularly in the shell gland (G. Gee, pers. comm.). Although the right ovary regresses early in the course of embry- onic development, the left ovary remains functional.

During maturation follicles are generally cate- gorized according to size and the presence and color of the yolk. In Galliformes, the smallest follicles visible on the surface of the ovary (about 0.2-1.0 cm in diameter) are termed small white follicles. As the small white follicle increases in diameter, a stage is reached when yellow yolk becomes visible. These events proceed without significant gonadotropin support. At the time of egg production, follicular oocytes have developed into a hierarchial arrange- ment, with the Fl follicle destined to ovulate and the F2 follicle second in the succession of daily ovulations. Once the follicle has been "recruited" into this hierarchy, the gonadotropin support be- comes critical, with FHS and LH providing stimu- lation of steroid production and regulation of factors that modulate growth, development, and finally ovulation of the follicle.

246 JOURNAL OF AVIAN MEDICINE AND SURGERY

2

3

Figure 2. A photomicrograph of a section of a testicle from a turkey showing the seminiferous epithelium and inter- stitial space. The seminiferous epithelium consists of spermatogonia (g), spermatocytes (y), spermatids (t), and Sertoli cells (s). The interstitial space contains Leydig cells (1), capillaries, and some connective tissue elements.

Figure 3. A scanning electron micrograph of turkey sperm on the surface of the ovum. The fibrous reticulum is the inner perivitelline layer, the investment the sperm must penetrate to fertilize the ovum.

Morphologically, the yellow yolk follicle in the rapid growth stage consists of a number of cellular and acellular layers surrounding the yolk. The peri- vitelline layer is an acellular fibrous layer homolo- gous to the mammalian zona pellucida. The gran- ulosa cell layer, which is a monolayer of cuboidal cells, surrounds the oocyte with cytoplasmic projec- tions that interconnect adjacent granulosa cells as well as form junctional complexes with the surface of the oocyte. The defined granulosa cell basement membrane is nearly 1 p~m thick. The theca interna,

theca externa, and the germinal epithelium consti- tute the remaining cell layers. The thecal and gran- ulosa cells are the primary sources of the steroids produced by the ovary; small follicles that are in initial stages of development (primary follicles) produce proportionally greater amounts of estradiol, and large follicles (F1-F3) produce high concentra- tions of progesterone.

Progesterone secreted by the large follicles stim- ulates the preovulatory surge in gonadotropins. Generally, only the Fl follicle ovulates with each

OTTINGER AND BAKST-AVIAN REPRODUCTIVE ENDOCRINOLOGY 247

daily ovulatory cycle, which in Galliformes is about 26 hours. This cycle of oviposition is followed by ovulation within 60 minutes and oviposition again 26 hours later. The cycle continues until the hen "rests" for a day at the end of a clutch or set of eggs laid sequentially. Photoperiod appears to be the major factor in determining the end of the clutch and in setting the timing for the first egg of the next clutch. The length of the clutch varies individually and with the strain of chicken. For example, heavy strains of chickens tend to have shorter clutches than the leghorn hen, which is a light strain selected for egg production. (For a more comprehensive re- view of ovulation in the hen, see Etches68.)

The egg and its transit through the reproductive tract

At oviposition, the chicken egg contains the ovum, which if fertilized possesses a 60,000-cell embryo just at the onset of forming the individual germ layers. Morphogenetic development of the chicken and turkey embryo during its 25 hours in the oviduct and through the first 8-12 hours of in- cubation was first categorized into discrete stages in the chicken by Eyal-Giladi and Kochav,69 and then by Gupta and Bakst70 in the turkey.

The yolk is primarily lipid and proteins suspend- ed in an aqueous phase. The albumen (egg white) is largely protein, which is secreted by the subepi- thelial tubual glands in the magnum region of the oviduct, and contains enzymes and some antibac- terial proteins (for detailed information, see Etch- es68). There is increased water content with aging that contributes to the larger egg size. Finally, the egg is surrounded by shell membranes and shell, which is composed of a mineral matrix.

The oviduct is a muscular tube through which the ovum travels to reach the shell gland. After the ovum is released from the ovary, it is "caught" by the funnellike end of the oviduct, the fibriated part of the infundibulum. Sperm must be in the infun- dibulum if fertilization is to occur. Regardless if fer- tilized or not, the ovum traverses the distal half of the infundibulum where it accrues some albumen before entering the magnum. Additional albumen is deposited, with regulation of protein production by estradiol. After about 3 hours in the magnum, the "egg mass" enters the isthmus where in 2-3 hours the shell membrane is formed. The egg mass then enters the shell gland, also referred to as the uterus. Shell formation occurs through a 19-20 hour pro- cess of calcite crystallization, which is largely under the control of progesterone.

The vagina functions as a conduit between the

shell gland and cloaca at oviposition. However, with respect to the process of reproduction, the vagina plays an essential role. Shortly after insemination (and copulation) the vaginal lumen "selects" only a relatively small number of sperm for transport to the sperm-storage tubules located in the anterior end of the vagina. These select sperm enter the sperm- storage tubules and are gradually released over a period of days in some species, or weeks in other species (see Bakst et a171). Sperm released over the course of the daily ovulatory cycle can ascend to the site of fertilization at the infundibulum and fer- tilize the daily succession of ova (Fig. 3).

Summary

A variety of rhythms affect animals, including seasonal, circadian, daily, and short-term rhythms. There are factors in the environment, including pho- toperiod and stressors such as disease, that impact on physiologic processes and disrupt rhythms. There are also more subtle factors such as nutrition that impact on reproductive capability. These have been studied in detail in poultry. Finally, the phys- iologic status of the animal and the process of mat- uration and aging also greatly affect the reproduc- tive response of the individual (for reviews, see Ot- tinger18,24). All these impact on the hypothalamus- pituitary-gonadal axis in the male and female bird and result in modulation of hypothalamic neuroreg- ulatory systems that alter GnRH synthesis and re- lease. A cascade effect follows that impacts on the reproductive status of the animal at all levels.

Acknowledgment: This is scientific article A7859, contribution 9189, of the Maryland Agri- culture Experiment Station. The authors thank Ms. Phyllis Bokman for her help in manuscript prepa- ration.

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Recommended Texts

Burley RW, Vadehra DV. The avian egg-chemistry and biology. New York: John Wiley & Sons, 1989.

Crawford RD. Poultry breeding and genetics. New York: Elsevier, 1990.