University of Nebraska - Lincoln
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1-1-1995
Endocrinology of the Avian Reproductive System
Mary Ann Ottinger
University of Maryland - College Park
Murray R. Bakst
U.S. 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. Paper 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 neuroendocrineregulation of hypothalamicand 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: reproductivebiology, endocrinesystem, accessory sex structures,birds
Introduction
organs. The ovulatory cycle relative to the oviduct
and its functions is also reviewed.
Avian species utilize a variety of reproductive
strategies that allow them to reproduce under a
diversity of conditions and environments. Endocrine and behavioral components of reproduction
are directed by the hypothalamus in response to
environmental triggers, such as photoperiod. Superimposed 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, pituitary 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 reproduction.
The purpose of this review is to provide an
overview of the male and female reproductive endocrine system in birds. This includes neuroendocrine regulation of hypothalamic and pituitary
gland hormones, gonadal function, and reproductive tract function. Emphasis is placed on the dynamics of the system and subsequent effects on
the function of the gonads and the accessory sex
Neuroendocrine Regulation of
Hypothalamic Processes and
Behavioral Responses
As in other vertebrates, the male and female avian
reproductive systems are regulated by the hypothalamus-pituitary-gonadal axis (Fig. 1). The hypothalamus 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 testosterone, 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 internal and external factors regulate and modulate hypothalamic 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 (cGnRH1).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 Maryland, College Park, MD 20742, USA (Ottinger), and the Germplasm and Gamete Physiology Laboratory, Agricultural Research
Service, U.S. Department of Agriculture, Beltsville, MD 20705,
USA (Bakst).
242
This article is a U.S. government work, and is not subject to copyright in the United States.
ENDOCRINOLOGY
OTINGERAND BAKST-AVIANREPRODUCTIVE
* Hypothalamus:
and
neuropeptides
neurotransmitters
regulatethe synthesisand
releaseof cGnRH-I.Potentialregulatory
peptides
includeVIP,Neuropeptide
Y,SubstanceP, and
the opioidpeptides.Inaddition,the monamines
havebeen implicated
in regulation
of cGnRH-I.
* Pituitary
Gland:Alphaandbetasubunitsare
LHand
synthesizedto producethe gonadotropins,
FSH. Production
of the mRNAforthese hormones
is regulatedbyGnRHandfurthermodulatedby
gonadalsteroids.
* The gonadsproducesteroidswhichfeed backto
the hyothalamus
to regulatecGnRH-lproduction
andsexualbehavior.The accessoryand
secondarysex structuresarealso dependenton
steroidhormonesupportfortheirmorphology
and
function.
243
Hypothraatrus
cGnRHCI
Pituitary Gland
LH
FSH
Gonads/Gamete Production
Testosterone
Estradiol/Progesterone
Accessory/Secondary Sex Structures
Oviducts/Vasdeferens
Comb/Wattleslothercharacteristics
Figure 1. A schematicdiagramof the avian hypothalamic-pituitary-gonadal
(HPG) axis, illustratingthe neuroendocrine regulationof hypothalamicand pituitarygland hormones,and their effect on reproductiveorgans.
species and phyla. Evidence points to the cGnRHII 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 mating behavior, with little role in the regulation of pituitary gland gonadotropins.9,10A role for GnRH as
a modulator of reproductive behavior has been hypothesized in some mammals, including voles.11
Their experiments provided convincing evidence
for the stimulation of male sexual behavior in castrated males given low levels of exogenous testosterone. We found similar effects in male quail. Castrated male quail given testosterone implants that
provide insufficient testosterone to stimulate sexual
behavior will show mating behavior for a short period of time in response to GnRH injection (CortesBurgos and Ottinger, unpubl. data). Additional intriguing data have been collected by Cheng and colleagues,12,13which showed that the GnRH system is
responsive to social cues and interactions, thereby
providing an additional level of environmental regulation 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 regulation 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 cGnRH-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 eminence, 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 cGnRH-I and little or no release of cGnRH-II.17
Stimulation of release by norepinephrine, which is
known to stimulate GnRH release, resulted in release 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 cGnRH-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, immunohistochemical 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.19-21Furthermore, the cGnRH-I system exhibits 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.22-26Other peptides, including vasotocin, vasoactive intestinal peptide, neuropeptide Y, and
opioid peptides have been implicated in the neuroendocrine regulation of GnRH, often because
neurons containing these peptides are in close anatomic proximity to cGnRH-I-containing neurons.
These peptides have been implicated through experimental 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, vasoactive intestinal peptide, and neuropeptide Y are
unclear. In summary, most evidence points to cGnRH-I as the endogenous hypothalamic hormone
critical for stimulating synthesis and release of pituitary 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 hypothalamic explants showed that GnRH release is
affected by sexual maturation.33-37Further, these
studies gave evidence for regulation of GnRH release 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.38,39However, 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 hypothalamic slices. This modification preserved
many of the connections between the cell bodies in
the preoptic and lateral septal regions with the axonal terminals in the median eminence.40 Subsequent 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 frequency of episodic release.38 Further, these catecholamines 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 inhibitory effect on cGnRH-I release, whereas short-term
estradiol exposure stimulated cGnRH-I release in
vitro.39 Conversely, opioid peptides, including metenkephalin and B-endorphin, acted in a dose-dependent 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 evidence for some of the regulatory elements that are
likely to be active in the avian hypothalamus. Interestingly, assays of cGnRH-I and catecholamines
show changes during the aging process.40 And finally, epinephrine concentrations were highly measurable in "punches" of avian hypothalamic areas
as compared with mammals in which epinephrine
levels are extremely low in the central nervous system (Ottinger et al., unpubl. data). This implies that
the avian system may use both norepinephrine and
epinephrine as well as a number of other neuropeptides 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. Lehrman's laboratory provided some of the first thorough studies of the linkages between hormones and
behavior in birds. Their early studies43,44provided
detailed descriptions of the behavioral patterns involved in courtship, mating, incubation, and parental care in the ring dove. Subsequent studies have
built upon this foundation and have characterized
the role of steroid hormones, prolactin, and neuropeptides 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 behavioral 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 hormone 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 counterpart, testosterone is required for avian male sexual
behavior and must be aromatized to its biologically
active metabolite, estradiol, in target areas in the
As in the regulation of
central nervous system.54',55
the endocrine portion of the reproductive axis, sex-
OTTINGER AND BAKST-AVIAN
ual behavior is also modulated by neuropeptides.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 effects 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 neuroendocrine and peptide regulation of sexual behavior 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 steroids, 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 secretagogues have been found effective in releasing
LH from dispersed pituitary gland cells.59 In addition, gonadotropins occur as chemical isoforms.60
This is potentially important as a mechanism for
more subtle regulation because of differing biological activity of the isoforms. At the molecular level,
the LH molecule is composed of an alpha and beta
subunit.61Further, 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 tubules, which contain Sertoli and germ cells (Fig. 2).
The Sertoli cells are responsive primarily to FSH
and, as in mammals, produce inhibin. Spermatogenesis has been recently reviewed elsewhere.63,64Dispersed between the seminiferous tubules are the androgen-producing cells--the Leydig cells. Once se-
REPRODUCTIVE ENDOCRINOLOGY
245
creted, testosterone, which is the major androgen
produced and secreted from the testes,65 is enzymatically reduced to its active metabolite, 5-alpha
dihydrotestosterone.65,66
Sperm are transported through a rudimentary epididymal region into the ductus deferens and stored
until ejaculation. Male birds do not possess accessory sex glands, which in mammals add fluid to the
sperm. Alternatively, when Galliformes ejaculate
the semen is mixed with a lymphlike transparent
fluid.63,64Nevertheless, 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 extender, 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 information on artificial insemination technology including semen collection, dilution evaluation, liquid
storage, and cryopreservation, see Bakst and Wishart67).
The Female System
The ovary of the reproductive female is remarkable 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 embryonic development, the left ovary remains functional.
During maturation follicles are generally categorized 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 arrangement, 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 becomes critical, with FHS and LH providing stimulation of steroid production and regulation of factors
that modulate growth, development, and finally
ovulation of the follicle.
246
JOURNALOF AVIAN MEDICINEAND SURGERY
2
3
Figure 2. A photomicrograph of a section of a testicle from a turkey showing the seminiferous epithelium and interstitial 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 perivitelline layer is an acellular fibrous layer homologous to the mammalian zona pellucida. The granulosa cell layer, which is a monolayer of cuboidal
cells, surrounds the oocyte with cytoplasmic projections 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~mthick. The theca interna,
theca externa, and the germinal epithelium constitute the remaining cell layers. The thecal and granulosa 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 concentrations of progesterone.
Progesterone secreted by the large follicles stimulates the preovulatory surge in gonadotropins.
Generally, only the Fl follicle ovulates with each
OTTINGERAND BAKST-AVIAN REPRODUCTIVEENDOCRINOLOGY
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 review of ovulation in the hen, see Etches68.)
247
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 spermstorage 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 fertilize the daily succession of ova (Fig. 3).
Summary
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 incubation 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 suspended in an aqueous phase. The albumen (egg white)
is largely protein, which is secreted by the subepithelial tubual glands in the magnum region of the
oviduct, and contains enzymes and some antibacterial proteins (for detailed information, see Etches68). 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 infundibulum if fertilization is to occur. Regardless if fertilized 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 process of calcite crystallization, which is largely under
the control of progesterone.
The vagina functions as a conduit between the
A variety of rhythms affect animals, including
seasonal, circadian, daily, and short-term rhythms.
There are factors in the environment, including photoperiod 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 physiologic status of the animal and the process of maturation and aging also greatly affect the reproductive response of the individual (for reviews, see Ottinger18,24).All these impact on the hypothalamuspituitary-gonadal axis in the male and female bird
and result in modulation of hypothalamic neuroregulatory systems that alter GnRH synthesis and release. A cascade effect follows that impacts on the
reproductive status of the animal at all levels.
This is scientific article
Acknowledgment:
A7859, contribution 9189, of the Maryland Agriculture Experiment Station. The authors thank Ms.
Phyllis Bokman for her help in manuscript preparation.
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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.