University of Nebraska - Lincoln

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

1995​
Endocrinology of the Avian

Reproductive System
Mary Ann Ottinger
University of Maryland -
College Park

Murray R. Bakst ​United

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

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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 ​Testicular discussed. ​are ​function ​discussed ​and ​relative ​the cellular
to egg ​bases formation
​ ​for spermatogenesis and
​ the hormonal ​and regulation
​ ​steroid production of
​ this
process. ​are also Key
​ words: reproductive biology, endocrine system, accessory sex structures, birds
hypothal- amus-pituitary-gonadal axis (Fig. 1).
The hypothal- amus produces a
gonadotropin-releasing hormone (GnRH) that
Introduction
stimulates pituitary gland production of
luteinizing hormone (LH) and follicle-stimulating
Avian species utilize a variety of reproductive
hormone (FSH), which in turn regulate ovarian
strategies that allow them to reproduce under a
and testicular function. Gonadal steroids,
diversity of conditions and environments. Endo-
primarily tes- tosterone, estradiol, and
crine and behavioral components of reproduction
progesterone return to the central nervous system
are directed by the hypothalamus in response to
through the bloodstream and provide a feedback
environmental triggers, such as photoperiod. Su-
regulation of hypothalamic GnRH production
perimposed on these triggers are internal factors
and release. Some additional in- ternal and
such as stage of the life cycle and general health.
external factors regulate and modulate hy-
The primary components of the "integrated"
pothalamic function. In this section, we review the
reproductive system are the hypothalamus, pitui-
regulation of GnRH in avian species, particularly
tary gland, and gonads. Accessory organs, which
in reference to regulation of the system in the
include the oviduct, excurrent duct system, and
associated cloacal structures, are also critical to breeding ​adult.
reproductive success. Moreover, endocrine and
behavioral components of reproduction must Gonadotropin-releasing hormone (GnRH)
function synchronously for successful reproduc-
In contrast to mammalian GnRH, two chemical
tion. The purpose of this review is to provide an forms of avian GnRH are known to exist: chicken
overview of the male and female reproductive en-
docrine system in birds. This includes neuroen- From the Department of Poultry Science, University of Mary-
docrine regulation of hypothalamic and pituitary land, College Park, MD 20742, USA (Ottinger), and the Germ-
plasm and Gamete Physiology Laboratory, Agricultural
gland hormones, gonadal function, and reproduc-
Research Service, U.S. Department of Agriculture, Beltsville,
tive tract function. Emphasis is placed on the dy- MD 20705, USA (Bakst).
namics of the system and subsequent effects on GnRH-I (cGnRH-I) and chicken GnRH-II
the function of the gonads and the accessory sex Since the discovery of these
organs. The ovulatory cycle relative to the oviduct (cGnRH- ​1).1,2 ​years ​
and its functions is also reviewed. hormones several ​
ago, some avian species have
been shown to have both cGnRH-I and
Neuroendocrine Regulation of Hypothalamic
cGnRH-II.3,4 Moreover, other forms of GnRH
Processes and Behavioral Responses
have been discovered in other
As in other vertebrates, the male and female
avian reproductive systems are regulated by the 242

This article is a U.S. government work, and is not subject to copyright in the United States.
AND BAKST-AVIAN REPRODUCTIVE ENDOCRINOLOGY 243
OTINGER ​

* ​the Hypothalamus: neurotransmitters have release include opioid been VIP, of peptides. cGnRH-I. implicated

Neuropeptide neuropeptides regulate In Potential

​ ​in addition, regulation Y, the Substance synthesis and regulatory
​ ​the of
monamines cGnRH-I. P, and peptides
​ ​and *​ ​Pituitary synthesized FSH. gonadal is regulated Production steroids. Gland:

to by produce GnRH Alpha of the and and the mRNA further beta gonadotropins, for subunits modulated these

hormones are LH by and *​ ​The the function. and secondary steroid hyothalamus sexual gonads hormone sex behavior.

produce structures support to regulate steroids The for are accessory their cGnRH-l also which morphology dependent
Gland
​
feed and production back on and to Hypothraatrus
​ cGnRHCI Pituitary
​ ​

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
very potent in stimulating a large amplitude
cGnRH-I release, but these neurochemicals did
riods.22-26 Other peptides, including vasotocin,
not affect the frequen- cy of episodic release.38
va- soactive intestinal peptide, neuropeptide Y,
Further, these catechol- amines were found to act
and opioid peptides have been implicated in the
on the alpha and beta adrenergic receptor
neu- roendocrine regulation of GnRH, often
systems (Li et al., unpubl. data). Separate
because neurons containing these peptides are in
experiments demonstrated that exposure to
close ana- tomic proximity to
gonadal steroids for several hours exerted an
cGnRH-I-containing neurons. These peptides
inhib- itory effect on cGnRH-I release, whereas
have been implicated through ex- perimental
short-term estradiol exposure stimulated
effects on the reproductive system.27-31 Studies
cGnRH-I release in vitro.39 Conversely, opioid
of neuroregulatory effects of these peptides
peptides, including met- enkephalin and
provide evidence that opioid peptides inhibit the
B-endorphin, acted in a dose-depen- dent
GnRH system, whereas the effects of vasotocin,
inhibitory manner and depressed both baseline
va- soactive intestinal peptide, and neuropeptide
and norepinephrine-stimulated cGnRH-I release
Y are unclear. In summary, most evidence points
with reduced amplitude of the episodic
to c- GnRH-I as the endogenous hypothalamic
release.41,'42 To summarize, these studies
hormone critical for stimulating synthesis and
provide additional insight into the regulation of
release of pi- tuitary gland LH and FSH, and this
cGnRH-I release in the sexually maturing and
GnRH action is mediated by calcium.14,32
mature bird. The adrenergic
As mentioned earlier, investigators have also used
systems appear to be important in stimulation of
in vitro methods to further elucidate regulation of
cGnRH-I release, whereas opioid peptides appear
cGnRH-I release in birds. Early studies with hy-
to inhibit cGnRH-I release. These results provide
pothalamic explants showed that GnRH release is
ev- idence for some of the regulatory elements
affected by sexual maturation.33-37 Further,
that are likely to be active in the avian
these studies gave evidence for regulation of
hypothalamus. In- terestingly, assays of cGnRH-I
GnRH re- lease by norepinephrine and other
and catecholamines show changes during the
peptides in vitro, presumably in a manner similar
aging process.40 And fi- nally, epinephrine
to their apparent ​roles in vivo. We also examined concentrations were highly mea- surable in
"punches" of avian hypothalamic areas as
cGnRH-I release in ​ vitro.38,39 However, our compared with mammals in which epinephrine
experiments differed from those previously levels are extremely low in the central nervous
conducted in two respects. First, cGnRH-I was sys- tem (Ottinger et al., unpubl. data). This
specifically measured with a highly sensitive and implies that the avian system may use both
specific enzyme immunoassay and second, our norepinephrine and epinephrine as well as a
dissections produced longitudinal hy- pothalamic number of other neuropep- tides to regulate
slices. This modification preserved many of the cGnRH-I production and release.
connections between the cell bodies in the
preoptic and lateral septal regions with the ax- Courtship and mating behavior
onal terminals in the median eminence.40 Subse-
quent experiments with these modifications There is a large body of literature on the vast
showed that challenge with regulatory peptides, diversity of reproductive behavior in birds and
including norepinephrine and epinephrine, were 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 demonstrated et ​a129,30).
that Studies testosterone in the and zebra its
metabolites finch have
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
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-
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
246 JOURNAL OF AVIAN MEDICINE AND SURGERY
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.
2

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.

layer homolo- gous

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
​ 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 membrane
 1 p~m thick. follicles) produce proportionally greater amounts
of the oocyte. is nearly The defined ​
The ​ theca ​ interna, of estradiol, and large follicles ​(F1-F3) produce
granulosa ​ cell ​ basement ​
theca externa, and the germinal epithelium high concentra- tions
​ of progesterone.
consti- tute the remaining cell layers. The thecal Progesterone secreted by the large follicles stim-
and gran- ulosa cells are the primary sources of ulates the preovulatory surge in gonadotropins.
the steroids produced by the ovary; small follicles Generally, only the Fl follicle ovulates with each
that are in initial stages of development (primary
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 course species of (see the Bakst daily et ovulatory ​a171). Sperm
​ cycle released can
ascend over the 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
All these impact on the hypothalamus- ​
individual (for reviews, see Ot- tinger18,24). ​ 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 ​ration.
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Recommended Texts

Burley RW, Vadehra DV. The avian egg-chemistry and

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Crawford RD. Poultry breeding and genetics. New
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