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
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 longlived 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, i)
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 axis22,31,32. 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.
BirdsIn 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.
MammalsIn 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 shortday 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. 1Photoperiodic 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 coincidence60,65 (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 (argininephenylalanine-amide) kisspeptin and RFRP3 (RF-amide
related peptide 3) are the regulators of hypothalmo-

Fig. 2Molecular 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 (TSH) 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 (PTTSH) 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 PTTSH 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.
References
1

Martinet L, Mondain-Monval M & Monnerie R, Endogenous

circannual rhythms and photorefractoriness of testis activity,
moult and prolactin concentration in mink (Mustella vison),
J Reprod Fertility, 95 (1992) 325.
2
Gwinner E, Bird migration: Its control by endogenous
clocks, in Frontiers of Life, Vol. 4: The living world, edited
by D Baltimore, R Dulbecco, F Jacob & R Levi-Montalcini,
(Academic Press, New York), 2001, 193.
3
Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K &
Ohtsu T, Circannual control of hibernation by HP complex in
the brain, Cell, 125 (2006) 161.
4
Gwinner E, Circannual rhythms in birds, Curr Opin
Neurobiol, 13 (2003) 770.
5
Farner D S & Follett B K, Light and other environmental factors
affecting avian reproduction, J Anim Sci, 25 (1966) 90.
6
Kumar V, Photoperiodism in higher vertebrates: An adaptive
strategy in temporal environment, Indian J Exp Biol,
35 (1997) 427.
7
Misra M, Rani S, Singh S & Kumar V, Regulation
of seasonality in the migratory male black headed
bunting (Emberiza melanocephala), Reprod Nutr Dev, 44
(2004) 341.
8
Hazlerigg D G & Wagner G C, Seasonal photoperiodism
in vertebrates: From coincidence to amplitude, Trends
Endocrinol Metab, 17 (2006) 83.
9
Dixit A S & Singh N S, Photoperiod as a proximate factor
in control of seasonality in the subtropical male tree sparrow,
Passer montanus, Front Zool, 8 (2011) 1.
10 Garner W W & Allard H A, Effect of relative length of day
and night and other factors of the environment on growth and
reproduction in plants, J Agric Res, 18 (1920) 533.

417

11 Kriegsfeld L J, Ranalli N J, Bober M A & Nelson R J,

Photoperiod and temperature interact to affect the GnRH
neuronal system of male prairie voles (Microtus ochrogaster),
J Biol Rhythms, 15 (2000) 306.
12 Kumar V, Singh S, Misra M & Malik S, Effects of duration
and time of food availability on photoperiodic responses
in the migratory male blackheaded bunting (Emberiza
melanocephala), J Exp Biol, 204 (2001) 2843.
13 Scheuerlein A & Gwinner E, Is food availability a circannual
zeitgeber in tropical birds? A field experiment on stonechats
in tropical Africa, J Biol Rhythms, 17 (2002) 171.
14 Dawson A, The effect of temperature on photoperiodically
regulated gonadal maturation, regression and moult in
starlings potential consequences of climate change, Funct
Ecol 19 (2005) 995.
15 Singh J, Budki P, Rani S & Kumar V, Temperature alters
the photoperiodically controlled phenologies linked with
migration and reproduction in a night-migratory songbird,
Proc R Soc B, 279 (2012) 509.
16 Baker J R, The evolution of breeding seasons, in Evolution:
Essays on aspects of evolutionary biology, edited by G R De
Beer, (Clarendon Press, Oxford, UK) 1938, 161.
17 Hahn T P, Integration of photoperiodic and food cues to
time changes in reproductive physiology by an opportunistic
breeder, the Red Crossbill Loxia curvirostra (Aves:
Carduelinae), J Exp Zool, 272 (1995) 213.
18 O'Brien S & Hau M, Food cues and gonadal development
in tropical spotted antbirds, J Ornithol, 147 (2005) 332.
19 Buenning E, Circadian rhythms and time measurement
in photoperiodism, Cold Spring Harb Symp Quant Biol,
25 (1960) 249.
20 Elliott J A, Stetson M H & Menaker M, Regulation of testis
function in golden hamsters: A circadian clock measures
photoperiodic time, Science, 178 (1972) 771.
21 Follett B K & Maung S L, Rate of testicular maturation, in
relation to gonadotrophin and testosterone levels, in quail
exposed to various artificial photoperiods and to natural
daylengths, J Endocrinol, 78 (1978) 267.
22 Follett B K & Sharp P J, Circadian rhythmicity in
photoperiodically induced gonadotrophin release and
gonadal growth in the quail, Nature, 223 (1969) 968.
23 Goldman B D, Mammalian photoperiodic system: formal
properties and neuroendocrine mechanisms of photoperiodic
time measurement, J Biol Rhythms, 16 (2001) 283.
24 Hamner W M, Diurnal rhythm and photoperiodism
in testicular recrudescence of the house finch, Science,
142 (1963) 1294.
25 Kumar V, Jain N & Follett B K, The photoperiodic clock in
blackheaded buntings (Emberiza melanocephala) is mediated
by a self-sustaining circadian system, J Comp Physiol A,
179 (1996) 59.
26 Rani S & Kumar V, Time course of sensitivity of the
photoinducible phase to light in the redheaded bunting,
Emberiza bruniceps, Biol Rhythm Res, 30 (1999) 555.
27 Singh S, Misra M, Rani S & Kumar V, The photoperiodic
entrainment and induction of the circadian clock regulating
seasonal responses in the migratory blackheaded bunting
(Emberiza melanocephala), Chronobiol Int, 19 (2002) 865.
28 Gwinner E, Uber die synchronization circannualer rhythmen
bie vogelen vogelvarte, 29 (1977) 16.
29 Chandola A, Bhatt D, & Pathak V K, Environmental
manipulation of seasonal reproduction in spotted munia

418

30

31

32
33

34

35

36

37

38

39

40
41

42

43

44

45

46

47

INDIAN J EXP BIOL, MAY 2014

Lonchura punctulata, in Avian endocrinology: Environmental

and ecological perspectives, edited by S Mikami, (Japan Sci
Soc Press, Tokyo/ Springer Verlag, Berlin) 1983, 229.
Gwinner E & Scheuerlein A, Seasonal changes in day-length
intensity as a potential zeitgeber of circannual rhythms in
equatorial stonechats, J Ornithol, 139 (1998) 407.
Farner D S & Gwinner E, Photoperiodicity, circannual and
reproductive cycles, in Avian endocrinology, edited by
A Epple & M H Stetson, (Academic Press, New York)
1980, 331.
Sharp P, Photoperiodic regulation of seasonal breeding in
birds, Ann NY Acad Sci, 1040 (2005) 189.
Okano T & Fukada Y, Phototransduction cascade and
circadian oscillator in chicken pineal gland, J Pineal Res, 22
(1997) 145.
Kojima D & Fukada Y, Non-visual photoreception by a
variety of vertebrate opsins, Novartis Found Symp, 224
(1999) 265.
Siopes T D & Wilson W O, Extraocular modification of
photoreception in intact and pinealectomized Coturnix, Poult
Sci, 53 (1974) 2035.
Davies D T & Follett B K, The neuroendocrine control
of gonadotrophin release in the Japanese quail. II. The role
of the anterior hypothalamus, Proc R Soc Lond B, 191
(1975) 303.
Benoit J, Le role des yeux dans laction stimulante de la
lumiere sure le developpement testiulaire chez le canard,
C R Soc Biol (Paris), 118 (1935) 669.
Menaker M & Keatts H, Extraretinal light perception in
the sparrow. II. Photoperiodic stimulation of testis growth,
Proc Natl Acad Sci USA, 60 (1968) 146.
Foster R G, Follett B K & Lythgoe J N, Rhodopsin-like
sensitivity of extraretinal photoreceptors mediating the
photoperiodic response in quail, Nature, 313 (1985) 50.
Bellingham J & Foster R G, Opsins and mammalian
photoentrainment, Cell Tissue Res, 309 (2002) 57.
Halford S, Pires S S, Turton M, Zheng L, GonzalezMenendez I, Davies W L, Peirson S N, Garcia-Fernandez J M,
Hankins M W & Foster R G, VA opsin-based photoreceptors
in the hypothalamus of birds, Curr Biol, 19 (2009) 1396.
Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S,
Hirunagi K, Ebihara S, Kubo Y & Yoshimura T,
A mammalian neural tissue opsin (Opsin 5) is a deep
brain photoreceptor in birds, Proc Natl Acad Sci USA, 107
(2010) 15264.
Freedman M S, Lucas R J, Soni B, von Schantz M, Muoz
M, David-Gray Z & Foster R, Regulation of mammalian
circadian behavior by non-rod, non-cone, ocular
photoreceptors, Science, 284 (1999) 502.
Davidson A J, Yamazaki S & Menaker M, SCN: ringmaster
of the circadian circus or conductor of the circadian
orchestra? Novartis Found Symp, 253 (2003) 110.
Tarttelin E E, Bellingham J, Hankins M W, Foster R G &
Lucas R J, Neuropsin (Opn5): A novel opsin identified in
mammalian neural tissue, FEBS Lett, 554 (2003) 410.
Kumar V & Follett B K, The circadian nature of melatonin
secretion in Japanese quail (Coturnix coturnix japonica),
J Pineal Res, 14 (1993) 192.
Brandstaetter R, Kumar V, Vant Hof T & Gwinner E,
Seasonal variation of in vivo and in vitro melatonin

48

49

50

51

52

53

54

55

56

57

58

59

60

61

62

production in a passeriform bird, the house sparrow (Passer

domesticus), J Pineal Res, 31 (2001) 120.
Gwinner E, Hau M & Heigl S, Melatonin: generation
and modulation of avian circadian rhythms, Brain Res Bull,
44 (1997) 439.
Reiter R J, Photoperiod: Its importance as an impeller of
pineal and seasonal reproductive rhythms, Int J Biometeorol,
24 (1980) 57.
Lincoln G A, Administration of melatonin into the
mediobasal hypothalamus as a continuous or intermittent
signal affects the secretion of follicle-stimulating hormone
and prolactin in the ram, J Pineal Res, 12 (1992) 135.
Follett B K, Davies D T & Gledhill B, Photoperiodic control
of reproduction in Japanese quail: changes in gonadotropin
secretion on first day of induction and their pharmacological
blockade, J Endocrinol, 74 (1977) 449.
Meddle S L & Follett B K, Photoperiodically driven changes
in Fos expression within the basal tuberal hypothalamus
and median eminence of Japanese quail, J Neuroscience,
17 (1997) 8909.
Kumar V, Jain N, Singh B P & Kumar B S, Plasma levels of
luteinizing hormone in intact and castrated blackheaded
bunting (Emberiza melanocephala) exposed to stimulatory
and nonstimulatory photoperiods, Reprod Nutr Dev, 33
(1993) 143.
Ubuka T, Bentley G E, Ukena K, Wingfield J C & Tsutsui K,
Melatonin induces the expression of gonadotropin-inhibitory
hormone in the avian brain, Proc Natl Acad Sci USA, 102
(2005) 3052.
Bentley G E, Jensen J P, Kaur G J, Wacker D W, Tsutsui K
& Wingfield J C, Rapid inhibition of female sexual behavior
by gonadotropin-inhibitory hormone (GnIH), Horm, Behav,
49 (2006) 550.
Yasuo S, Watanabe M, Takagi T, Iigo M, Ebihara S &
Yoshimura T, Photoinducible phase-specific light induction
of Cry 1 gene in the pars tuberalis of Japanese quail,
Endocrinol, 145 (2004) 1612.
Tamarkin L, Westrom W K, Hamill A I & Goldman B D,
Effect of melatonin on the reproductive systems of male and
female Syrian hamsters: A diurnal rhythm in sensitivity to
melatonin, Endocrinol, 99 (1976) 1534.
Goldman B D, Darrow J M, & Yoge L, Effect of timed
melatonin infusions on reproductive development in
Dungarian hamster (Phodopus sungorus), Endocrinol, 114
(1984) 2074.
Weaver D R & Reppert S M, Melatonin receptors are present
in the ferret pars tuberalis and pars distalis, but not in brain,
Endocrinol, 127 (1990) 2607.
Lincoln G, Messager S, Andersson H & Hazlerigg D,
Temporal expression of seven clock genes in the
suprachiasmatic nucleus and the pars tuberalis of the sheep:
evidence for an internal coincidence timer, Proc Natl Acad
Sci USA, 99 (2002) 13890.
Johnston J D, Tournier B B, Andersson H, Masson-Pvet
M, Lincoln G A & Hazlerigg D G, Multiple effects of
melatonin on rhythmic clock gene expression in the
mammalian pars tuberalis, Endocrinol, 147 (2006) 959.
Messager S, Garabette M L, Hastings M H & Hazlerigg
D G, Tissue-specific abolition of Per1 expression in the
pars tuberalis by pinealectomy in the Syrian hamster.
Neuroreport, 12 (2001) 579.

RANI et al.: PHOTOPERIODIC REGULATION OF SEASONAL REPRODUCTION

63 Dardente H, Menet J S, Poirel V J, Streicher D, Gauer F,

Vivien-Roels, B, Klosen, P, Pvet, P & Masson-Pvet M,
Melatonin induces Cry1 expression in the pars tuberalis of
the rat, Brain Res Mol Brain Res, 114 (2003)101.
64 Lincoln G A, Andersson H & Loudon A, Clock genes in
calendar cells as the basis of annual timekeeping in mammalsa unifying hypothesis, J Endocrinol, 179 (2003) 1.
65 Bell-Pedersen D, Cassone V M, Earnest D J, Golden S S,
Harding P E, Thomas T L & Zoran M, Circadian rhythms
from multiple oscillators: lessons from diverse organisms,
Nat Rev Genet, 6 (2005) 544.
66 Klosen P, Sbert M, Rasri K, Laran-Chich M P &
Simonneaux V, TSH restores a summer phenotype in
photoinhibited mammals via the RF-amides RFRP3 and
kisspeptin, The FASEB, 27 (2013) 2677.
67 Pathak V K & Chandola A, Seasonal variation in circulating
thyroxine and tri-iodothyronine concentration in spotted
munia, Lonchura punctulata, Gen Comp Endocrinol,
50 (1983) 201.
68 Pant K & Chandola-Saklani A, Relative role of T4 and T3 in
the migratory physiology of redheaded bunting, J Comp
Physiol, 163 (1995) 389.
69 Dawson A & Thapliyal J P, The thyroid and photoperiodism,
in Avian endocrinology, edited by A Dawson & C M Chaturvedi,
(Narosa Publishing House New Delhi, India) 2001, 141.
70 Benoit J, Role of the thyroid in the gonado-stimulation by
artificial light in the domestic duck, C R Soc Biol Paris, 123
(1936) 243.
71 Woitkevitsch A A, Dependence of seasonal periodicity in
gonadal changes in the thyroid gland in Sturnus vulgaris,
L.C.R. (Doklady) Acad Sci URSS, 27 (1940) 741.
72 Follett B K & Nicholls T J, Influences of thyroidectomy and
thyroxine replacement on photoperiodically controlled
reproduction in quail, J Endocrinol, 107 (1985) 211.
73 Shi Z D & Barrell G K, Requirement of thyroid-function
for the expression of seasonal reproductive and related
changes in red deer (Cervus elaphus) stags, J Reprod Fertil,
94 (1992) 251.
74 Parkinson T J & Follett B K, Thyroidectomy abolishes
seasonal testicular cycles of Soay rams, Proc R Soc Lond Ser
B Biol Sci, 259 (1995) 1.
75 Anderson G M & Barrell G K, Out-of-season breeding in
thyroidectomised red deer hinds, Proc New Zealand Soc
Animal Production, 58 (1998) 20.
76 Freeman D A, Teubner B J, Smith C D & Prendergast B J,
Exogenous T3 mimics long day lengths in Siberian hamsters,
Am J Physiol Regul Integr Comp Physiol, 292 (2007) R2368.
77 Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T,
Hirunagi K & Ebihara S, Light-induced hormone conversion
of T4 to T3 regulates photoperiodic response of gonads in
birds, Nature, 426 (2003) 178.
78 Lechan R M & Fekete C, Role of thyroid hormone
deiodination in hypothalamus, Thyroid, 15 (2005) 883.
79 Yasuo S, Watanabe M, Nakao N, Takagi T, Follett B K,
Ebihara S & Yoshimura T, The reciprocal switching of two
thyroid hormone-activating and -inactivating enzyme genes
is involved in the photoperiodic gonadal response of
Japanese quail, Endocrinol, 146 (2005) 2551.
80 Watanabe T, Yamamura T, Watanabe M, Yasuo S, Nakao N,
Dawson A, Ebihara S & Yoshimura T, Hypothalamic
expression of thyroid hormone activating and inactivating
enzyme genes in relation to photorefractoriness in birds

81

82

83

84

85

86

87

88

89

90

91

92
93

419

and mammals, Am J Physiol Regul Integr Comp Physiol,

292 (2007) 568.
Yasuo S, Nakao N, Ohkura S, Iigo M, Hagiwara S, Goto A,
Ando H, Yamamura T, Watanabe M, Watanabe T, Oda S,
Maeda K, Lincoln G A, Okamura H, Ebihara S & Yoshimura
T, Long-day suppressed expression of type 2 deiodinase
gene in the mediobasal hypothalamus of the Saanen goat, a
shortday breeder: implication for seasonal window of thyroid
hormone action on reproductive neuroendocrine axis,
Endocrinol, 147 (2006) 432.
Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y,
Murai A, Ebihara S, Korf H W & Yoshimura T, Involvement
of thyrotropin in photoperiodic signal transduction in mice.
Proc Natl Acad Sci USA 105 (2008) 18238.
Hanon E, Lincoln G A, Fustin J M, Dardente H,
Masson-Pevet M, Morgan P J & Hazlerigg D G, Ancestral
TSH mechanism signals summer in a photoperiodic
mammal, Curr Biol, 18 (2008) 1147.
Herwig A, Wilson D & Logie T J, Photoperiod and acute
energy deficits interact on components of the thyroid
hormone system in hypothalamic tanycytes of the Siberian
hamster, Am J Physiol, 296 (2009) R1307.
Yamamura T, Hirunagi K, Ebihara S & Yoshimura T,
Seasonal morphological changes in the neuro-glial
interaction between gonadotropin-releasing hormone nerve
terminals and glial endfeet in Japanese quail, Endocrinol,
145 (2004) 4264.
Yamamura T, Yasuo S, Hirunagi K, Ebihara S & Yoshimura T,
T3 implantation mimics photoperiodically reduced encasement
of nerve terminals by glial processes in the median eminence
of Japanese quail, Cell Tissue Res, 324 (2006) 175.
Jansen H T, Cutter C, Hardy S, Lehman M N &
Goodman R L, Seasonal plasticity within the gonadotropinreleasing hormone (GnRH) system of the ewe: changes in
identified GnRH inputs and glial association, Endocrinol,
144 (2003) 3663.
Nakao N, Ono H, Yamamura t, Anraku T, Takagi T, Higashi
K, Yasuo S, Katou Y, Kageyama S & Uno Y, Thyrotropin in
the pars tuberalis triggers photoperiodic response, Nature,
452 (2008) 317.
Wittkowski W, Bergmann M, Hoffmann K & Pera F,
Photoperiod-dependent changes in TSH-like immunoreactivity
of cells in the hypophysial pars tuberalis of the Djungarian
hamster, Phodopus sungorus, Cell Tissue Res, 251
(1988) 183.
Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero
H, Pvet P & Masson-Pvet M, The mt1 melatonin receptor
and RORb receptor are co-localized in specific TSHimmunoreactive cells in the pars tuberalis of the rat pituitary,
J Histochem Cytochem, 50 (2002) 1647.
Rodriguez E M, Blazquez, J L, Pastor F E, Pela B, Pena P,
Peruzzo B & Amat P, Hypothalamic tanycytes: a key
component of brain-endocrine interaction, Int Rev Cytol, 247
(2005) 89.
Dardente H, Wyse C, Birnie M, Dupr S, Loudon A, Lincoln
G & Hazlerigg D G, A molecular switch for photoperiod
responsiveness in mammals, Curr Biol, 20 (2010) 2193.
Bentley G E, Tucker S, Chou H, Hau M & Perfito N,
Testicular growth and regression are not correlated with Dio2
expression in a wild male songbird, Sturnus vulgaris,
exposed to natural changes in photoperiod, Endocrinol, 154
(2013) 1813.