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Photoperiodic regulation of seasonal reproduction in higher vertebrates

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Indian Journal of Experimental Biology
Vol. 52, May 2014, pp. 413-419

Mini Review

Photoperiodic regulation of seasonal reproduction in higher vertebrates

Sangeeta Rani1* & Vinod Kumar2
DST IRHPA Center for Excellence in Biological Rhythm Research
1
Department of Zoology, University of Lucknow, Lucknow 226 007, India
2
Department of Zoology, University of Delhi, Delhi 110 007, India

Long-lived animals such as birds and mammals adapt readily to seasonal changes in their environment. They integrate
environmental cues with their internal clocks to prepare and time seasonal physiological changes. This is reflected in several
seasonal phenotypes, particularly in those linked with migration, hibernation, pelage growth, reproduction and molt. The
two endocrine secretions that play key roles in regulating the seasonal physiology are melatonin and thyroid hormone.
Whereas, melatonin is used as an endocrine index of day length (and consequently duration of night), the seasonal up- and
down-regulation of thyroid hormone affects the physiology, perhaps by influencing different pathways. Both of these
hormones are shown to act via a ‘photoperiodic axis’ constituted by the photoreceptors, hypothalamus and pituitary. Recent
studies have revealed that the pars tuberalis that connects hypothalamus and pituitary, locally synthesizes the thyroid
stimulating hormone (TSH) in response to light (birds) or melatonin (mammals). The levels of TSH regulate the DIO2 and
DIO3 synthesis in the ependymal cells in hypothalamus, and in turn affect the release of gonadotropin releasing hormone.
This review mainly focuses on the current understanding of the mechanisms of photoperiodic regulation of seasonal
responses in the higher vertebrates.

Keywords: Birds, DIO2, DIO3, Melatonin, Photoperiodism, Thyroid

The environment exerts selection pressure on long-
lived animals such as birds and mammals. Because of
its predictable seasonality, these animals synchronize
their annual life history stages with the seasonal
environment resulting in optimal survival and success
strategies. Endogenous clocks help to anticipate
changes in the environment, prepare animals for
such changes and bring about seasonal changes in
physiology and behaviour, namely migration,
hibernation, pelage growth, reproduction and molt1-3.
These clocks run on their own with a period close to 1
year; hence they are called circannual clocks4 (circa =
about; annum = year). In natural environment,
however, they are synchronized with the cyclicity of
the external environment. Thus the onset of seasonal
phenotypes is virtually precise over the years.
Of all the environmental factors, day length
(photoperiod) is possibly the most important and
reliable cue. It has been shown to be involved in
regulation of seasonal cycles of reproduction and
associated functions in several avian and mammalian
species5-9. This is described as photoperiodism10.
Animals respond to the photoperiod (long or short)
——————
Correspondent author
Telephone: 91 522 2740423
E-mail: sangeetarani7@yahoo.com
to breed at a time in the year when the survival of
the young ones is maximized. Accordingly, animals
with short gestation periods (e.g. birds) breed during
summer, and those with long gestation period
(e.g. sheep) breed during the winter. These animals
are thus called long day and short day breeders,
respectively.
Besides photoperiod, food and temperature are
also known to affect and regulate the seasonal
responses11-15. It has been suggested that all these
factors have distinct roles in regulation of annual
cycles. By-and-large, the photoperiod acts as a
proximate factor initiating the seasonal responses
in time, whereas food may act as the ultimate factor
affecting actual time of the seasonal response, e.g.
reproduction16,17. At times, however, the distinction
between roles of proximate and ultimate factors could
be diffuse18.
Circadian basis of photoperiodic induction
The interaction between the photoperiod and
‘circadian’ clock (circa= about, dies, a day) that
‘reads’ the successive phases of light and dark19, leads
to the photoperiodic response. The critical photoperiod
that induces the photoperiodic response is species
specific. For example, for gonadal stimulation to
occur it may be >12 h in hamster20 or >11.5 h in
414 INDIAN J EXP BIOL, MAY 2014
quail21 and bunting7. In bunting, the induction of body
mass occurs at relatively shorter photoperiods than
required for the gonadal growth suggesting that the
critical photoperiod is also response specific7.
Generally the photoperiodic response is explained
on the basis of ‘external coincidence’ model that
postulates the existence of an endogenous circadian
rhythm of photosensitivity (CRP) of which the portion
during subjective day is insensitive to light and that in
the subjective night is sensitive or photoinducible22.
When the light falls in the photoinducible phase (phi, φi)
the long day response would occur23. The circadian
basis of photoperiodic response has been demonstrated
by several protocols such as night interruption
and resonance (where the light exposure of CRP
during photoinducible phase results in a photoperiodic
response) in hamster, quail and bunting23-27.
The circadian clocks that regulate the daily
rhythms and circannual clocks that regulate the
seasonal responses are self-sustained and allow the
organisms to anticipate changes in the environment4.
Both are synchronized by the photoperiod and
light intensity. In birds28,29 the shortening of annual
photoperiodic cycles results in corresponding shortening
of the gonadal and molt cycles. Also, the cyclic
changes in day light intensity could synchronize the
gonadal and molt cycles30. The circadian clocks are
synchronized by the day and night cycles whereas
the circannual clocks keep a track of changes in
photoperiod from long days in summer to short days
in winter. However, compared to circadian clocks, the
circannual oscillators are considered weak and their
period length is much less conserved.
The ‘photoperiodic axis’
The seasonal response (e.g. reproduction) is
regulated by the interaction of photoperiod with the
neuroendocrine components namely hypothalamus,
pituitary and gonad (HPG) that together constitute
the ‘photoperiodic axis’22,31,32. As studied in different
birds and mammals, the photoperiodic axis is activated
during breeding season. The photoperiod perceived by
the photoreceptors induces the GnRH neurons in the
hypothalamus to release the gonadotropin releasing
hormone (GnRH) that in turn causes the secretion of
gonadotropins (luteinizing hormone, LH and follicle
stimulating hormone, FSH) from the pituitary gland,
which stimulate the gonads to recrudesce.
The photoreception in birds occurs at three levels;
the eye, pineal and deep brain photoreceptors (DBP).
The role of these photoreceptors in regulation of
seasonal response has been demonstrated in several
bird species33,34. The photoreception at these sites is
independent of each other as pinealectomy35 and
suprachaismatic nucleus (SCN) lesion in quail36 and
enucleation in ducks37 did not affect the photoperiodic
response. In sparrow, the injection of India ink
underneath the head skin abolished the gonadal
recrudescence38 and direct illumination of hypothalamus
initiated the gonadal growth in quail maintained under
short days39. All these photoreceptors have an opsin
based photoreceptive molecule39,40. Distinct opsins
have been identified in the brains of different bird
species34,41,42.
In mammals, unlike birds, eyes are the only
photoreceptors and their removal abolishes the
photoperiodic response43. Light information from the
eyes reaches the suprachiasmatic nucleus the master
oscillator in mammals44 and from here the signals
reach the pineal gland via superior cervical ganglion
(SCG) (Fig. 1). Thus the melatonin secretion from
pineal gland in mammals is under the control of SCN.
Recently, the discovery of expression of Neuropsin
(a mammalian orthologue of OPN5) in brain and
spinal cord of mammals has opened up alternatives to
eyes alone being the photoreceptors45.
Phototransduction pathway
Irrespective of having different photoreceptors, and
different action phases (diurnal or nocturnal),
melatonin is secreted only during night in both birds
and mammals. It decodes the daily changes in light
and dark hours as well as duration of dark hours in
different seasons; winter or summer46,47. In birds, the
seasonal responses are independent of melatonin
rhythm27,48, however, in mammals melatonin is the
key element in regulation of the seasonal responses49
as shown by studies where pinealectomy abolished
and melatonin administration restored the seasonal
response50.
Birds—In quail a single long day could induce
the gonadal axis as shown by the expression of
immediate early gene (c-fos) in the mediobasal
hypothalamus (MBH) and increased secretion of
luteinizing hormone (LH)51,52. These effects were
independent of melatonin secretion53 although the
melatonin receptors and gonadotropin inhibitory
hormone (GnIH) have been co-localized in the
paraventricular (PVN) region that sends fibers to
median eminence (ME)54. Studies have shown that
GnIH inhibits gonadotropin release55 and abolition
of melatonin rhythm lowers the GnIH levels54. This
 RANI et al.: PHOTOPERIODIC REGULATION OF SEASONAL REPRODUCTION
suggests a possible role for melatonin in the
regulation of seasonal reproduction in birds.
However, in birds, the expression profile of the
two clock genes, period 2 (Per2) and cryptochrome
1 (Cry1) is not melatonin dependent, rather it is
photoperiod dependent56.
Mammals—In stimulated hamsters under long
days, the daily melatonin administration in the late
afternoon or before dawn resulted in gonadal
regression57. Similarly, timed administration of
melatonin in pinealectomized hamsters induced short-
day responses58. It has been found that the pars
tuberalis (PT) but not the brain is the site of melatonin
receptors (type 1 melatonin receptor; MT1) abundant
in mammals59. The melatonin signals are associated
with the expression of clock genes in PT60,61 and no
Fig. 1—Photoperiodic regulation of seasonality in birds and
mammals. In birds, the light signals received by deep brain
photoreceptors (DBP) are sent to pars tuberalis (PT) via OPN5
positive CSF contacting neurons. In mammals, the light received
from the retinal photoreceptors (eyes), reaches the SCN which
sends signals to pineal gland to produce melatonin. The melatonin
acts on median eminence adjacent to pars tuberalis via melatonin
receptors (MT1). Once the signal reaches the PT, local production
of thyroid stimulating hormone (PT-TSH) is stimulated. PT-TSH
acts on the ependymal cells to induce DIO2 expression. DIO2
converts T4 into T3 which influences the GnRH secretion and
thus activates the hypothalamo-pituitary-gonadal (H-P-G) axis
resulting into gonadal response.
415
circadian gene expression occurs in the pinealectomised
hamsters or transgenic mice that lacked MT162.
In mammalian PT, the melatonin induces
expression of cryptochorme 1 (Cry 1) in early night
and that of period 1 (Per1) at the end of night63.
Thus, the onset and offset of melatonin signal regulate
the expression of Cry1 and Per1 independently.
Therefore, the photoperiod dependent melatonin
duration leads to a change in timing of their
peak expression64. The alteration of the seasonal
phasing of these two core clock genes, leads to their
‘internal coincidence’60,65 (Fig. 2a). The interconnected
transcription-translational loops and their effects on
the expression of clock genes regulate the circadian
responses65. However, not much is known about the
molecular machinery in PT that regulates the seasonal
responses in mammals. Recently, in mammals, it
has been demonstrated that the RF-amide (arginine-
phenylalanine-amide) kisspeptin and RFRP3 (RF-amide
related peptide 3) are the regulators of hypothalmo-
Fig. 2—Molecular coincidence models to explain the regulation of
seasonal responses. Internal coincidence model (upper panel; 2a)
suggests that the melatonin signal during short days
(long nights; left panel) and long days (short nights; right panel)
affects the elements of the molecular clockwork. Increasing
melatonin in the evening induces expression of Cry, whereas
falling levels of melatonin at dawn promote expression of Per.
The duration of night thus changes the phase relation of the clock
genes (internal coincidence) and leads to the summer phenotype.
External coincidence model (lower panel; 2b) postulates that
melatonin affects the Eya3 expression. Independent of day length,
Eya3 expression peaks ~12 h after dark and melatonin onset. Thus
under short days, its peak time falls at night when the melatonin
level is high which suppresses the Eya3 expression, whereas,
under long days, the peak time for Eya3 expression falls during
the day when melatonin level is minimal, that result in its high
expression. This model suggests that melatonin synchronizes the
expression of Eya3 by direct suppression. Thus the circadian
rhythms interact with a light-dependent stimulus and lead to the
photoperiodic response.
416 INDIAN J EXP BIOL, MAY 2014
pituitary-gonadal axis that stimulate the GnRH
neurons. Both of them are down regulated by the
melatonin suggesting a regulatory role for melatonin
in seasonal reproduction66.
Role of thyroid hormones
Besides melatonin and GnIH, various studies also
suggest that thyroid hormones (TH) T3 (tri-iodothyronin)
and T4 (tetra-iodothyronin) also play important
roles in the regulation of seasonal responses67-69.
Although the major form of circulating thyroid
hormone is T4; it is T3 that is biologically active.
That the thyroidectomy affects seasonal reproduction
has been shown in several birds and mammals70-74.
The function could be restored by exogenous
administration of TH75,76.
Light during photoinducible phase induces the
gonadal response. It is speculated that during this
time, some molecular events must be taking place
in the MBH. The T3 and T4 concentration in MBH
were found to increase manifold under long days,
while their levels in general circulation were similar
under both short and long days. This suggested that
on long day exposure, T3 and T4 are synthesized
locally in the MBH area. The two enzymes type 2
deiodinase (DIO2) and type 3 deiodinase (DIO3)
synthesized in the ECs lining the III ventricle in MBH
region77 are responsible for fine tuning the local levels
of T3 and T478. Long days up-regulate DIO2 that
converts T4 into T3 and short days up-regulate DIO3,
that converts T4 and T3 into inactive reverse T3
(rT3) and 3, 3’ diiodothyronine (T2) respectively79.
The intra-cerebroventricular (ICV) infusion of T3
under short days induced the testis growth in a
dose-dependent manner, whereas infusion of DIO2
inhibitor under long days inhibited the testis growth77.
Thus the local activation of thyroid hormones seems
to have functional significance. The photoperiodic
induction of DIO2 and DIO3 has been shown in some
birds and mammals80-84.
Besides the molecular changes, the photoperiod
induced structural changes in the GnRH nerve
terminals and glial endfeet were also observed at ME;
the site of TH receptors85. During short days, the
GnRH neuron terminals were not in contact with
basal lamina due to the structural arrangement of glial
endfeet, whereas long days could help establish this
contact. T3 has been found to alter this structural
arrangement as its administration in quail under short
days yields similar results86. The seasonal changes
in GnRH neurons and the glial cells have also been
observed in ewe87. Thus the T3 induces structural
changes in GnRH neuron and glial cells regulate the
seasonal reproduction in birds and mammals.
The pars tuberalis thyrotropin (PT-TSH)—As
discussed above, the local synthesis of T3 and T4 in
the hypothalamus is regulated by DIO2 and DIO3.
The microarray data on quail has shown that in PT,
long days induce the expression of the first wave of
genes, of which one encodes for thyroid stimulating
hormone beta subunit (TSHβ) and the other for
transcriptional co-activator eyes absent 3 (Eya3)88.
This is followed by the upregulation of DIO2 and
downregulation of DIO3 expression in ECs. The ICV
administration of TSH induces DIO2 expression and
the testis growth under short days. This suggests
that pars tuberalis TSH (PT–TSH) is the main
regulator of seasonal response in birds. Opsin-5
(OPN5) positive neurons project to the ME adjacent
to PT and are suggested to send light signals to PT
to induce TSH (Fig. 1).
In mammals, both melatonin and DIO2 and DIO3
play a crucial role in the regulation of seasonal
reproduction. Melatonin receptor 1 (MT1) is
found in PT that produces TSH89,90 but not in ECs
which is the site of DIO2 and DIO3 expression91. This
suggests that melatonin regulates the expression of
DIO2 and DIO3 via PT-TSH. The involvement
of the TSH signaling pathway in the melatonin
mediated regulation of DIO2 and DIO3 expression
was further confirmed when TSH receptor null
(TSHR-null) mice failed to respond to melatonin
administration82. Long day induced DIO2 expression
mediated by TSH is observed in short day breeders
such as sheep83 as well. Thus, PT-TSH mediates
the ‘time of the year’ information in both long day
and short day breeders which might be processed
differently for the two breeding strategies. Eya3
regulates the TSHb expression in PT via a circadian
transcriptional factor (thyrotropin embryonic factor;
TEF). Independent of day length, the Eya3 expression
peaks ~12 h after dark and the melatonin onset. Under
short days, its peak time falls at night when the
melatonin level is high, and that suppresses Eya3
expression whereas, under long days the peak time
for Eya3 expression is during the light hours
when melatonin level is minimum. Thus, melatonin
synchronizes the phase of Eya3 expression by its
direct suppression92. This can be explained by
‘external coincidence model’ where the circadian
 RANI et al.: PHOTOPERIODIC REGULATION OF SEASONAL REPRODUCTION
rhythm interacts with a light-dependent stimulus and
leads to the photoperiodic response (Fig. 2b).
Conclusion
It seems that despite having different structural
organizations, the avian and mammalian seasonal
responses are mediated by similar mechanisms
(Fig. 1). It has been found that in birds and mammals
the thyroid hormones are the key players. The PT-
TSH signaling pathway suggests that other hormonal
signals may also be involved in the regulation of
seasonal function. In mammals, it is the melatonin
dependent pathway that regulates seasonal responses
while in birds the light dependent pathway appears
to play a more direct role. However, recent report
on starling93 found no correlation of DIO2 with
photoperiod, and gonadal status indicating that the
mechanism of photoperiodic time measurement is
even more complex than proposed. Although, the core
mechanism of photoperiodic time measurement in
both birds and mammals is the light reception
followed by a cascade of downstream events, there
is much more to be explored to understand the
photoperiodic regulation of seasonal events.
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