Avian Endocrinology
A Dawson & C M Chaturvedi (Eds)
Copyright  2001 Narosa Publishing House, New Delhi, India
Photoperiodic control of seasonal
reproduction: neuroendocrine mechanisms
and adaptations
P Deviche and T Small
Department of Biology, Arizona State University, Tempe, AZ 852871501, USA
Introduction
Over 75 years ago, Rowan (51) used dark-eyed juncos, Junco hyemalis,
to demonstrate that changes in ambient photoperiod can profoundly
affect the activity of the reproductive system. Many subsequent
investigations have confirmed and extended this original finding. It is
now established that, in many birds living at middle and high latitudes,
exposure to long days (LD, approximately 12 or more hours of light)
stimulates the hypothalamo-pituitary-gonadal axis, increasing the
secretion of gonadotropins (luteinizing hormone, LH; follicle-stimulating
hormone, FSH), and induces gonadal growth (54, 56, 62). It is also
known that in most species, prolonged exposure to LD does not maintain
the activity of the reproductive system indefinitely: The system
eventually ceases to respond to LD and regresses. This phenomenon is
called photorefractoriness.
The hypothalamic peptide, gonadotropin-releasing hormone
(GnRH-I, hereafter referred to as GnRH; review, 11), plays a pivotal role
in mediating photoinduced reproductive development and in inducing
the ensuing gonadal regression that results from photorefractoriness. The
amount of GnRH in the hypothalamus, as assessed by semi-quantitative
immunocytochemistry or radioimmunoassay, is high in photosensitive
birds exposed to short days (SD) or LD, is greatly depressed in
chronically photorefractory birds when compared to photosensitive
birds, and is increased following subsequent exposure to SD and reestablishment of photosensitivity (12, 13, 14). The mechanism that
mediates alterations in GnRH-secreting cell function when birds become
photorefractory is poorly understood. Little is known also on the
contribution of changes in GnRH production versus release to the
regression of the reproductive system observed in photorefractory birds.
Not all species show similar responses to day length with respect to the
114 Avian Endocrinology
timing and extent of photorefractoriness, and in fact pioneering
investigations by Farner and colleagues (21) suggested that
photorefractoriness evolved more than once in birds.
In this article, we compare some well-studied experimental
models in terms of events occurring at the time of photorefractoriness
with particular emphasis on changes in GnRH activity. We use this
information to discuss how photorefractoriness may affect GnRH
production and release differently across species.
Photoinduced reproductive development and regression
In most avian species, the elevated activity of the reproductive system
that characterizes the breeding period is influenced by multiple
environmental factors such as day length, temperature, food availability,
mates in appropriate physiological condition, and a suitable breeding
habitat (63). Of these factors, day length has been shown in many cases
to be of paramount importance. Even desert species, such as zebra
finches, Taeniopygia guttata, that are thought to time breeding as a
function of rainfall and have traditionally been considered nonphotoperiodic, increase their reproductive system activity when exposed
to very long day length in captivity (2). Day length also influences the
reproductive physiology of spotted antbirds, Hylophylax naevioides, a
sedentary tropical species that is naturally exposed to relatively small
annual changes in photoperiod (32). Thus, the reproductive system of
most, and perhaps all, birds living over a wide range of latitudes from
arctic regions to the tropics (59) can presumably respond to changes in
day length.
Photic information affecting the avian hypothalamo-pituitary axis
is conveyed to this axis by extra-ocular and extra-pineal brain receptors
(60, reviews, 34, 44) that are generally referred to as deep encephalic
receptors. These receptors are believed to be located in or close to the
lateral septum and the tuberal hypothalamus regions of the brain (39,
64). In pigeons, Columba livia, encephalic photoreceptors have
biochemical characteristics resembling those of retinal rod/cones (58).
Neither the exact identity of these receptors nor their anatomical or
functional relationship with GnRH cells is known.
In typically photoperiodic species, photorefractoriness develops
during the summer, when day length is still well in excess of that
necessary to stimulate vernal gonadal development. Thus, a
characteristic of these species is that photoinduced cycles of gonadal
recrudescence followed with regression are asymmetrical with respect to
the summer solstice. Photoinduced gonadal regression in summer is
considered adaptive for at least two reasons. First, it curtails
reproduction in anticipation of a seasonal deterioration of ambient
Photoperiodic control of reproduction  Deviche and Small 115
conditions. Second, it permits the expression of other aspects of the
annual cycle including postnuptial molt, fattening, and migration, which
are energetically or otherwise incompatible with reproductive activities
(15, 35, 45). Photorefractoriness is mediated centrally and is not
consequent to an increased negative feedback of gonadal steroids on the
hypothalamo-pituitary axis or to an inability of the anterior pituitary to
respond to GnRH (38, 44). As discussed below, species may differ with
respect to the neuroendocrine events occurring at the end of the breeding
period, raising the question of whether there are fundamental species
differences in the processes that cause and possibly maintain
photorefractoriness.
Absolutely photorefractory species
At the end of a photoinduced gonadal cycle, species, such as the
European starling, Sturnus vulgaris, the house finch, Carpodacus
mexicanus, the dark-eyed junco, the white-crowned sparrow, Zonotrichia
leucophrys, and the male American tree sparrow, Spizella arborea,
become absolutely photorefractory. The photorefractory condition in
these species persists as long as birds remain exposed to LD. Dissipation
of photorefractoriness, i.e. restoration of photosensitivity as determined
by the ability to respond to LD with increased GnRH release, requires
exposure to SD. The neuroendocrine changes that result from
photorefractoriness have been examined in greatest detail in European
starlings. Photorefractoriness in starlings is associated with decreased
size and immunostaining intensity of hypothalamic GnRH perikarya, but
fiber staining in the median eminence does not decline until gonadal
regression is nearly complete (26). Reduced GnRH production in
starlings, therefore, constitutes an early indication that birds have
become photorefractory. At this time some GnRH may still be released
into the anterior pituitary, but not in amounts sufficient to sustain
elevated gonadotropin secretion and gonadal function. Consistent with
the idea that photorefractoriness in starlings inhibits GnRH production
prior to necessarily inhibiting the GnRH release mechanism, males
sampled during gonadal regression had reduced hypothalamic, but not
median eminence, expression of the precursor molecule for GnRH
(proGnRH-GAP) and of GnRH itself, compared to photostimulated
males (47). Median eminence staining for both peptides was reduced
only after regression was complete. The mechanism mediating the
decrease in GnRH production when birds become photorefractory is not
known. Parry and Goldsmith (46) found that GnRH cells of
photoregressed starlings receive increased synaptic input compared to
cells of birds that were undergoing photoinduced gonadal maturation.
However, no such increase occurred until gonadal regression was
complete. Thus, changes in synaptic input to GnRH cells may contribute
116 Avian Endocrinology
to maintaining starlings in the photorefractory state, although they are
probably not responsible for inhibiting the production of GnRH that is an
early consequence of photorefractoriness.
Less is known about the neuroendocrine changes associated with
the onset of photorefractoriness in other species. We recently
investigated this question in adult male dark-eyed juncos obtained from a
subarctic population. Juncos become photorefractory at the end of June,
after exposure to photoperiod exceeding 12 h (12 L) for approximately
four months. At this time LH concentrations and testis mass decline
rapidly (20), but this decline is not coupled to changes in the numbers of
hypothalamic proGnRH-GAP or GnRH cells, which do not differ from
those of fully photostimulated and photosensitive juncos (41). Similar
observations have been made in white-crowned sparrows (Meddle,
personal communication). They suggest that in these species, and
contrary to the situation in starlings, the decrease release of GnRH that is
observed in photorefractory birds does not result from decreased
hypothalamic production of the peptide. A recent investigation on whitecrowned sparrows extended this conclusion by investigating whether
photorefractory birds can acutely release physiologically effective
amounts of GnRH in response to pharmacological stimulation by the
excitatory glutamate agonist, N-methyl-D-aspartate (NMDA; (40)).
NMDA is thought to stimulate LH release by acting on GnRH-secreting
neurons (33). An injection of NMDA to photorefractory sparrows with
partially regressed testes rapidly increased plasma LH. This treatment
had a similar effect on LH when given to photostimulated sparrows,
suggesting that photorefractoriness in these birds (and in juncos) does
not deplete hypothalamic GnRH stores.
If photorefractoriness in juncos and sparrows caused an inhibition
of the GnRH release mechanism without concurrently depressing the
peptide production, GnRH would presumably accumulate in
hypothalamic cells. GnRH would then be found in higher amounts in
photorefractory birds than in photostimulated birds. That this has not
been observed using immunocytochemical methods suggests that
decreased GnRH release must somehow be coupled to declining GnRH
production, as is the case in starlings. Further experimentation, perhaps
using methods other than immunocytochemistry, is warranted to test this
hypothesis and to evaluate the extent to which changes in GnRH
production and release are temporally related as birds of various species
become photorefractory or regain photosensitivity. Research into the
above questions will also benefit from investigations on the extent to
which changes in hypothalamic GnRH expression follow changes in the
synthesis of proGnRH-GAP or the conversion of this peptide to GnRH.
Photoperiodic control of reproduction  Deviche and Small 117
Photorefractoriness in absolutely photorefractory birds kept on LD
for a prolonged period is generally associated with low hypothalamic
GnRH stores as measured by immunoreactive GnRH cell numbers or
sizes, intensity of immunostaining in these cells, or numbers or densities
of immunoreactive fibers (19, 52). The time course of this decrease has
not been determined, and we do not know to what extent it results from
intracellular degradation of GnRH or release of the peptide in small
amounts that do not induce a significant secretion of gonadotropins.
Relatively photorefractory species
The Japanese quail, Coturnix c. japonica, has proved to be an
exceptional model for many elegant studies on photoperiodic responses
(reviews, 22, 24). As is the case for absolutely photorefractory birds that
have regained photosensitivity, transfer of Japanese quail from SD to LD
rapidly activates the hypothalamo-pituitary-gonadal axis (23). Similarly,
the reproductive system of European quail, Coturnix coturnix, exposed
to natural photoperiod recrudesces when day length exceeds
approximately 12L (3). In contrast to the situation in absolutely
photorefractory species, Japanese quail that are chronically exposed to
fixed artificial LD do not undergo spontaneous gonadal regression,
which in this species requires some decrease in day length. In European
quail exposed to a natural photocycle, gonadal regression likewise
occurs in late summer, when photoperiod has declined from 18L: 6D to
about 14L: 10 D (3). Further, gonadal recrudescence in SD-regressed
quail starts immediately after transfer back to LD and is not preceded by
a period of unresponsiveness to LD (50). Quail are for this reason said to
be relatively photorefractory. Note that the definition of relative
photorefractoriness in quail differs from that in another species, the
house finch (31). Male house finches exposed to summer photoperiod
become absolutely photorefractory. The period of absolute
photorefractoriness in this species last for about 45 days and naturally
ends in September, when finches start to regain photosensitivity as
measured by their capacity to recrudesce testes in response to LD.
During this period birds are said to be relatively photorefractory because
exposure to day length exceeding, but neither equal to nor shorter than
that to which they were previously exposed, is necessary to stimulate
gonadal development. Male finches exposed to natural photoperiod and
sampled at the end of October, when they had presumably regained
photosensitivity to very long days and were relatively photorefractory,
had reduced brain GnRH expression compared to breeding birds (6).
The neuroendocrine events associated with photostimulation in
quail have been studied in considerable detail (7, 39, 48), but the changes
in GnRH function taking place during relative photorefractoriness are
118 Avian Endocrinology
not well known. Foster et al. (25) found GnRH expression in brain
regions including the preoptic area of quail exposed to SD for 25 days
and with regressed gonads to be higher than in chronically LD-exposed
birds. GnRH release in these birds may cease following transfer to SD,
allowing the peptide to accumulate within brain cells.
The question of whether absolute and relative photorefractoriness,
as defined in the quail, represent extremes of a continuum or two
fundamentally different mechanisms has been debated by several authors
(10, 29, 44) and remains unsolved. This issue has been addressed by
investigating species, such as the house sparrow, Passer domesticus, that
may not strictly follow the above-described pattern of absolute or
relative photorefractoriness. Male house sparrows exposed to LD for a
sufficiently long time become photorefractory, as shown by the fact that
their GnRH expression declines and their gonads regress (10, 29).
Further, males exposed to LD (17L: 7D) in September do not respond to
these LD (49), indicating that they are absolutely photorefractory.
However, males that are exposed to LD until around the summer
solstice, and then to artificially declining day length, can exhibit gonadal
regression earlier, and changes in brain expression of GnRH that are
intermediate, compared to birds not exposed to declining photoperiod (8,
29). Changes in gonad size in sparrows transferred from LD to shorter
day length thus resemble those seen in quail and superficially consistent
with the idea that sparrows become relatively, and then absolutely
photorefractory. To test this hypothesis, sparrows were photostimulated
by exposure to 18L: 6D and then transferred to shorter photoperiod (16L:
8D or 13: 11D) either after or before the onset of testicular regression
(10). Testicular regression rate in birds transferred to shorter photoperiod
after regression had begun was accelerated compared to that of males
that became absolutely photorefractory as a result of continued exposure
to 18L: 6D. In contrast, transfer from 18L: 6D to a shorter photoperiod
before the onset of gonadal regression did not affect regression. The data
suggest that photorefractoriness is programmed well in advance of
testicular regression, as is the case in white-crowned sparrows (42). The
results also argue against a period of relative photorefractoriness
preceding absolute photorefractoriness, supporting the view that absolute
and relative photorefractoriness represent two distinct mechanisms and
not extremes of a continuum.
Temporally flexible species
Photoperiod does not play an equally important role in the control of
breeding cycles in all species, some of which in fact exhibit considerable
reproductive flexibility and have extended or irregular breeding cycles
(30, 36). Flexibility is, for example, observed in species that live at low
Photoperiodic control of reproduction  Deviche and Small 119
latitudes and are normally exposed to small annual changes in
photoperiod compared to those residing at middle or at high latitudes.
Also, species, such as zebra finches, that inhabit xeric environments
where rainfall is rare and sporadic, may retain the capacity to respond to
changes in day length (2), but use primarily non-photic stimuli such as
precipitation and/or environmental changes associated with rainfall to
time their breeding activities.
The neuroendocrine bases of reproduction in temporally flexible
species have been best studied in crossbills (red crossbill, Loxia
curvirostra; white-winged crossbill, L. leucoptera). Crossbills feed
primarily on conifer seeds (1, 43), the production and availability of
which undergo large and irregular fluctuations from one year and one
region to another. The birds have adapted to this temporal and
geographical unpredictability by adjusting their breeding period to the
food supply. As a result, crossbills can breed throughout a large portion
of the year, starting at the end of winter and ending in late summer (1618, 28). It should be noted that even though crossbills have a longer
reproductive period than most middle and high latitude passerines, they
exhibit a well-defined seasonal reproductive pattern. They rarely breed
during autumn, when they are molting and their gonads are regressed,
even if their preferred food is locally abundant (16, 18, 28).
Seasonal changes in reproductive physiology in crossbills do not
result only from changes in food supply, because captive birds exposed
to a natural photocycle simulating natural conditions and receiving food
ad libitum exhibit seasonal cycles of plasma LH, gonadal size, and molt
(27). In these birds, testes recrudesce and circulating plasma LH
increases in the spring, concurrent with increasing day length. LH levels
decrease and gonadal regression occurs at the end of the summer and
early autumn (July-August), when molt begins. These results on captive
crossbills are consistent with data on free-living conspecific birds (17,
28), generally resemble those obtained in other passerines, and suggest
use of photoperiod to time reproductive recrudescence and regression.
Indeed, male red crossbills that were transferred from SD to LD had
higher circulating LH levels and enlarged testes compared to males held
on SD (27, 57). These studies also revealed two important aspects of the
crossbill reproductive physiology.
First, photoinduced LH secretion and testis mass development
were attenuated, although not eliminated, in chronically food-restricted
compared to ad libitum-fed and LD-exposed males, indicating an
important stimulatory effect of a non-photic cue – food availability – on
the reproductive system. Consistent with this observation, free-living
white-winged crossbills started to breed at the end of the winter, i.e.
when photoperiod was considerably less than 12L: 12D, following a
120 Avian Endocrinology
summer of high conifer seed production (18). In contrast, after a summer
of poor seed production, few or no birds bred locally until the following
summer, when a new crop of seeds became available.
Second, male red crossbills exposed to constant LD for over four
(57) or five (27) months did not become photorefractory, retaining large
gonads and elevated LH. In contrast, the gonads of captive birds held at
constant thermoneutral temperature, receiving food ad libitum, and
exposed to photoperiod simulating the natural cycle regressed after
exposure to day length exceeding 12L for approximately four months
(27). The failure of gonads to spontaneously regress despite continued
exposure to LD suggests that crossbills are relatively photorefractory:
Gonadal regression in the fall may require a decrease in day length, as is
the case in quail. Thus, crossbills apparently differ from other temperate
region passerines studied so far, which terminate breeding as a result of
absolute photorefractoriness.
Only one study has investigated the GnRH system of crossbills
(37). Here, captive male white-winged crossbills were held on a
naturally changing photoperiod and sacrificed in May, when they had
large testes, and then in October and January, when testes were small. It
was found that brain expression of GnRH underwent relatively small
temporal changes; the intensity of cellular immunostaining for GnRH
was lower in October than at other times, but neither the number of
GnRH cells nor the brain area containing GnRH fibers changed
seasonally. Thus, crossbills in the fall presumably retain relatively high
brain GnRH levels, but also have regressed gonads and low circulating
testosterone concentrations (18), suggesting that GnRH is not released.
At this time they rarely breed even in the presence of an abundant food
supply (16, 18, 28). In contrast, breeding can occur at the end of the
winter, when the food supply is not greater and day length is equal to or
shorter than in the fall, but brain GnRH content is presumably about the
same. What mechanism then prevents regular fall breeding by these
birds?
One hypothesis is that non-photic stimuli such as food and
possibly social factors must be present to induce release of GnRH at
concentration sufficient to fully activate the reproductive system, and the
sensitivity of the GnRH system to these stimuli varies seasonally.
Accordingly, birds have a low sensitivity to non-photic stimuli at the end
of the summer and during early fall, shortly after they have completed a
breeding cycle. At this time GnRH is present in hypothalamic cells, but
is not released in amounts sufficient to stimulate substantial LH and FSH
secretion. Thus, the reproductive system remains quiescent. With time
spent on SD during fall and early winter, birds become increasingly
sensitive to non-photic cues. If an adequate food supply remains
Photoperiodic control of reproduction  Deviche and Small 121
available, reproductive development starts and a breeding cycle is
initiated although day length may be shorter than in autumn and not yet
increasing. Consistent with this idea, free-living male white-winged
crossbills sampled during a fall and winter when spruce seeds were
abundant had elevated circulating LH and testosterone in November and
December, respectively, when day length was less than 8L and
decreasing (18). Crossbills that breed at the end of winter and early
spring can perhaps continue to do so during summer, when they are
photostimulated by LD, and pending the availability of sufficient food
(18). At this time and with the occurrence of shorter days, gonads finally
regress and molt begins. Prolactin is a likely candidate in the mediation
of autumnal gonadal regression. Secretion of prolactin in free-living
male white-winged crossbills gradually increases during summer and
early fall (18). The increase is presumably photoinduced, as has been
found in other species that terminate breeding by developing relative (4)
or absolute (9, 53, 55) photorefractoriness. Prolactin is not considered to
cause photorefractoriness (review, 34), but it exerts antigonadal effects
(5, review, 53) and in European starlings has been implicated in the
control of postnuptial molt (13).
Fig. 1 presents a generalized model of the relative roles of
photoperiodic and non-photoperiodic factors in the development of the
reproductive system in temporally flexible breeders. It is assumed that
GnRH is present in the brain year-round, but its release in amounts
sufficient to effectively stimulate the pituitary-gonadal axis above a
minimum threshold depends on the additive effects of photoperiodic and
non-photoperiodic (food quality and availability, precipitation or factors
associated with rainfall, etc, depending on the species) factors. When
gonads are regressed at the end of a breeding cycle (e.g. autumn), the
GnRH system is resistant to stimulation, and GnRH is normally not
released in significant amounts. The sensitivity of the GnRH system to
stimulation by these factors then gradually increases (e.g. late winter)
and reproductive development can occur if non-photoperiodic factors
provide sufficient stimulation, even though photoperiod is short and by
itself ineffective. Finally, the stimulatory influence of photoperiod
becomes sufficiently strong (e.g. summer) to induce reproductive
development despite weak, but still necessary stimulation by nonphotoperiodic factors.
It should be noted that the proposed role of non-photic factors on
the GnRH system may not differ fundamentally from that used by
typically photoperiodic and less flexible species which time reproductive
development based primarily on day length. In these species, restoration
of photosensitivity after absolute photorefractoriness is gradual, a
function of the time spent on SD (61), and associated with a build up of
122 Avian Endocrinology
hypothalamic GnRH stores (12). Once photosensitivity has been partially
or completely regained, release of these stores is induced most easily by
exposure to sufficiently long days. Species that breed on a flexible
schedule have retained sensitivity to photoperiod in that LD activates
their reproductive system, but in addition they have evolved an unusually
high sensitivity to specific non-photoperiodic factors. By responding
reproductively to these factors even when photoperiod is very short, such
as at the end of the winter, crossbills, for example, can take advantage of
a specialized resource, conifer seeds, which is frequently available in
sufficient amount on an irregular temporal and spatial basis.
Combined Stimulus for
Reproduction
High
Minimum threshold
High
High
Low
Low
Low
Autumn
Late Winter
Summer
Fig. 1 Schematic representation of the relative contributions of
photoperiod (lower part of columns) and of non-photic cues (upper part of
columns) to the development of the reproductive system in temporally
flexible species. The figureFigure
shows
the minimum threshold that need to be
1 Deviche and Small
reached for stimulation of the hypothalamo-pituitary-gonadal axis in
response to day length and to two levels (low, high) of non-photic
stimulation. See text for further information.
Conclusions
A lot of our current knowledge on the neuroendocrine bases of avian
photoperiodism is derived from investigations on a few well
characterized and absolutely photorefractory species. Investigations on
species such as quail, as well as examination of the natural diversity of
avian reproductive patterns (36), suggest that photoperiod is critical to
the activity of the hypothalamo-pituitary-gonadal axis. However, strict
Photoperiodic control of reproduction  Deviche and Small 123
reliance on photoperiodic information to regulate seasonal reproductive
cycles, although probably widespread, is not the only, and perhaps not
the most common, mechanism used by birds. Recent and limited work
on species, such as crossbills, that reproduce on a flexible and variable
seasonal schedule, has revealed that environmental stimuli other than
photoperiod can profoundly affect the reproductive system. Much
remains to be discovered about the very nature of these stimuli, their
interaction with photoperiod in the control of the activity of the
hypothalamo-pituitary-gonadal axis, and the neural pathways by which
they affect neuroendocrine functions, in particular the GnRH system.
It has long been known in photosensitive birds that the threshold
for physiological responses to photic information, and the magnitude of
these responses, is not constant, but rather variable. This threshold is
higher in birds that have just regained photosensitivity than in birds that
are fully photosensitive as a result of prolonged exposure to SD. Recent
data on crossbills, which can also respond to photoperiod, suggest that
the same applies to non-photic cues. Accordingly, gonadal cycles in
species exhibiting reproductive plasticity must be considered to result
from complex interactions between photoperiod and non-photoperiodic
factors to which these species are sensitive, but also from the temporally
variable impact of these factors, itself a function of the physiological
condition of the individual.
Acknowledgments
The authors thank Dany Pierard and Michael Moore for comments on an
early version of the manuscript, and Christy Strand and Madhusudan
Katti for valuable discussions during its preparation.
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