Physiology& Behavior, Vol. 48, pp. 403--408. ©Pergamon Press plc, 1990. Printed in the U.S.A.
0031-9384/90 $3.00 + .00
Photoperiodic Responsiveness in House Mice
R A N D Y J. N E L S O N l
Department of Psychology, The Johns Hopkins University, Baltimore, MD 21218
R e c e i v e d 2 April 1990
NELSON, R. J. Photoperiodicresponsivenessin housemice. PHYSIOL BEHAV 48(3) 403-408, 1990.--House mice (Mus musculus)
and laboratory strains of rats (Rattus norvegicus) have been traditionally considered nonphotoperiodic because their reproductive
systems are unaffected by day length (photoperiod). In rats, however, at least three experimental manipulations, perinatal testosterone
injection, chronic peripubertal testosterone exposure, or peripubertal olfactory bulbectomy, have revealed latent reproductive
photoperiodism. The effectiveness of these experimental treatments may be unique to albino rats. Alternatively, these experimental
manipulations may unmask the ability to discriminate short from long days in several "nonphotoperiodic" species and, thus, reveal
clues to common physiological mechanisms underlying reproductive responsiveness to photoperiod. In the present study, male house
mice were 1) subjected to olfactory bulbectomy or a sham operation at 23 days of age, 2) injected with testosterone or the oil vehicle
at 3 days of age, or 3) implanted subcutaneously with an empty Silastic capsule or one filled with testosterone at 22 days of age. All
mice were subsequently housed either in LD 16:8 or LD 4:20 photoperiods. The physiological mechanisms necessary to discriminate
long from short day lengths are extant in house mice. Testicular mass was significantly reduced in short-day bulbectomized males when
assessed 6 weeks postoperatively, but not when measured 10 weeks after surgery. Similarly, mice injected with testosterone when 3
days old and reared in short days had smaller testes as compared to testosterone-treated males housed in long days. Mice implanted
with testosterone capsules regressed their reproductive systems regardless of photoperiod. Other reproductive organ weights followed
the same general pattern of results as for testicular mass. Body mass was not affected by day length. Taken together, these results
indicate that mice process photoperiodic information, but that it is normally uncoupled from reproduction. These data also suggest that
it may be more appropriate to categorize traits, not individuals or species, as responsive to photoperiod.
Photoperiodism
Reproduction
Testosterone
Day length
MANY species limit reproduction to a specific time of the year.
Regardless of when mating occurs, offspring typically are produced during the spring or summer when food availability is high
and other environmental conditions are most conducive to survival
(14). Some populations of animals begin breeding directly in
response to the availability of adequate food (13). However, the
appearance of sufficient food to support reproduction occurs too
late in the breeding season to be useful for initiating reproduction
for individuals of many temperate or boreal zone species because
of the time constraints imposed by gametogenesis and pregnancy. Mechanisms have evolved to physiologically anticipate
adequate food availability by relying on other environmental cues
that reliably predict food availability. Day length, or photoperiod,
has high predictive value for individuals of many mammalian
species (4).
Species that phase their seasonal reproductive cycles by measuring day length have been termed "photoperiodic" (6). Typically, the gonads and sexual accessory tissues of photoperiodresponsive rodents regress, gonadal and pituitary hormone secretion
wanes, and mating behavior stops when the animals are maintained in short photoperiods (14,22); i.e., photoperiods in which
the duration of light/day is below a critical minimum of approximately 10-12 hr light/day. In several rodent species, the gonads
spontaneously redevelop after prolonged maintenance in short
photoperiods (26). The laboratory cycle of short-day reproductive
regression and spontaneous recrudescence corresponds with the
species' annual cycle of breeding in nature (17,27). Reproductive
responsiveness to short days is prevented by removal of the pineal
gland (9,10).
Other species have traditionally been considered "nonphotoperiodic" because manipulation of photoperiod does not affect
reproductive competence. Thus, Norway rats (Rattus norvegicus),
house mice (Mus musculus), and guinea pigs (Cavia porcellus)
kept in short photoperiods maintain large functional gonads and
sire offspring (3, 7, 12, 21). However, four different treatments
have revealed latent photoperiodism in laboratory rats (16, 18, 23,
25). Male rats bearing subcutaneous testosterone implants displayed some testicular regression when housed in short days, but
not in long photoperiods (25). Similarly, neonatal injections of
testosterone slowed gonadal growth in short-day reared male rats
as compared to their long-day counterparts (23). Removal of the
olfactory bulbs also unmasked reproductive responsiveness to
short photoperiods (16,18). Olfactory-bulbectomized rats discriminated long from short day lengths via a circadian mechanism
functionally similar to that possessed by photoperiodic species in
that the phase of light and not its duration determined physiological interpretation of day length on the reproductive system (15).
Moderate restriction of food intake reduced reproductive organ
1Electronic mail should be addressed: [email protected].
403
404
NELSON
mass when paired with short, but not long, days (20). In all four
paradigms, prior removal of the pineal gland blocked reproductive
responsiveness to short days.
The physiological means by which early testosterone treatment
or olfactory bulbectomy affect the expression of photoperiodism
are unknown. The extent to which these photoperiodic mechanisms are unique to laboratory rats or representative of other
reproductively nonresponsive species is also unknown. The present
study addressed the effect of three manipulations, viz., olfactory
bulbectomy, neonatal, and peripubertal testosterone treatment, on
reproductive photoperiodic responsiveness in house mice. It was
hypothesized that physiological manipulations that reveal reproductive photoperiodic responsiveness in rats would also unmask
photoperiodic responsiveness in house mice.
METHOD
Housing Conditions
Adult male and female house mice (Mus musculus) (CF1,
Charles River) were shipped to our laboratory. Mating pairs were
established and housed in LD 16:8 (16 hr light/day; lights on 0600
hr EST) photoperiods at 21---2°C and a relative humidity of
5 0 _+ 10%. Food (Agway Prolab 1000, Syracuse, NY) and tap
water were provided ad lib. Animals were housed in polypropylene cages (27.8 × 7.5 × 13 cm). Two weeks after insemination,
pairs were maintained either in LD 16:8 or LD 4:20 photoperiods.
Male offspring were assigned to one of the testosterone treatment
conditions (described below).
Other CF1 male mice were obtained from Charles River at 21
days of age. Upon arrival in our laboratory these animals were
housed in groups of 3 in polypropylene cages (27.8 × 7.5 × 13 cm)
for one day. These males were subjected to olfactory bulbectomy
or to a sham operation at 23 days of age and housed either in LD
16:8 or LD 4:20 day lengths until the end of the experiment.
Surgical Procedures
At 23 days of age, male mice were anesthetized with an
intraperitoneal injection of a mixture of ketamine (50 mg/kg),
rompun (5 mg/kg), and acepromazine (5 mg/kg) and randomly
assigned to one of two surgical manipulations: olfactory bulbectomy or a sham operation. After surgery, animals were randomly
assigned to long or short day length conditions. Sample sizes for
the resulting four experimental groups were: short-day bulbectomized mice=22, short-day sham-operated mice= 22, long-day
bulbectomized mice = 22, and long-day sham-operated mice = 22.
Half of these animals in each surgical treatment group were killed
six weeks postoperatively, and the remaining animals were killed
10 weeks postoperatively.
Olfactory bulbectomies were performed by drilling a 2.5 mm
hole medially just posterior to the nasal-frontal suture. After the
bulbs were visualized they were removed by aspiration. The
resulting hole was packed with Gelfoam and the skin sutured. The
sham-operated mice received a 2.5 mm hole drilled medially and
posterior to the nasal-frontal suture. The bulbs were visualized,
hemostasis was achieved by direct pressure and the scalp incision
sutured. Animals recovered from surgery in their home cages
warmed to 35°C by thermostatically controlled heating pads.
Testosterone Treatment
Male mice were injected with testosterone (1 mg) (Sigma, St.
Louis, MO) suspended in sesame seed oil (0.1 cc) or the oil
vehicle alone at 3 days of age. Males were weaned at 21 days of
age and individually housed thereafter either in LD 16:8 or LD
4:20 photoperiods for 6 weeks (LD 16:8, testosterone injected:
n = 3 0 ; LD 4:20, testosterone injected: n = 2 0 ; LD 16:8, oil
injected: n = 28; LD 4:20, oil injected: n = 26).
Other male mice were obtained from Charles River at 21 days
of age. The next day they were weighed, anesthetized with
methoxyflurane vapors, and implanted subcutaneously with Silastic capsules (10 mm of testosterone packed into a 15 mm Silastic
capsule; o.d. = 0.318 cm; i.d. = 0.157 cm) that either were empty
or filled with testosterone (Sigma). Mice were individually housed
either in LD 16:8 or LD 4:20 photoperiods (LD 16:8, testosterone
implant: n = 22; LD 4:20, testosterone implant: n = 2 2 ; LD 16:8,
empty implant: n = 1 8 ; LD 4:20, empty implant: n = 2 0 ) , then
killed 9 weeks later.
Autopsy Procedures
All animals were killed by cervical dislocation. Mice were
weighed. Paired testes, epididymides, seminal vesicles, and epididymal fat pads were dissected at autopsy and weighed.
Paired testes (capsule removed) and epididymides were minced
with dissecting scissors, separately transferred to an Eberbach
blender, and homogenized for 30 and 45 sec, respectively (8). The
number of sperm-shaped cells resistant to homogenization was
determined in duplicate for each homogenate in a hemocytometer
under phase-contrast microscopy. The average was used to compute the final number of sperm per paired organ.
Statistical Analyses
Comparisons among groups for each experimental parameter
were analyzed with an overall analysis of variance (SAS General
Linear Model for unbalanced ANOVA, Version 5, 1985). Individual pair-wise comparisons were analyzed with independent
two-tailed t-tests. The treatment effects were considered statistically significant if p<0.05. All analyses involved planned comparisons; consequently, no post hoc correction factors were
necessary (11).
Protocols from studies on rats were followed as closely as
possible resulting in different termination ages. Consequently, all
data were corrected for body mass prior to being subjected to
ANOVA. Absolute values were also compared within cells (i.e.,
different aged animals were not compared) and are presented in
graphs and tables.
RESULTS
Testes
Male house mice possess the ability to discriminate long from
short day lengths. At nine weeks of age (6 weeks postsurgery), the
testes of olfactory bulbectomized mice housed in short days
weighed less than those of bulbectomized mice in long days
(p<0.01), and less than those of sham-operated mice housed in
either photoperiod (p<0.01 in both cases) (Fig. 1). Exposure to
short days did not affect testicular mass in sham-operated mice.
Photoperiod also did not influence the reproductive condition of
animals maintained an additional four weeks in their respective
experimental conditions (p>0.05) (Fig. 1).
Perinatal injection of testosterone also revealed photoperiodic
responsiveness in male house mice. Short-day mice injected with
testosterone at 3 days of age had smaller testes at nine weeks of
age as compared to short-day animals receiving perinatal injections of sesame seed oil (p<0.01) (Fig. 1). The testes of
testosterone-injected short-day mice also weighed less than the
gonads of long-day mice injected either with oil or testosterone
when 3 days old (p<0.01 in both cases) (Fig. 1).
Male mice maintained in LD 4:20 photoperiods and bearing
subcutaneous Silastic capsules of testosterone had smaller testes
PHOTOPERIODISM IN HOUSE MICE
than short-day or long-day mice beating empty capsules 00<0.01
in each case) (Fig. 1), but did not differ significantly from mice
chronically exposed to testosterone and LD 16:8 photoperiods
00>0.05).
Photoperiod did not affect testicular sperm numbers 00>0.05 in
all cases). However, bulbectomized mice examined six weeks
postsurgery had significantly fewer sperm than sham-operated
mice 00<0.01) (LD 4:20, bulbectomized mice = 11.74- 1.67; LD
16:8, bulbectomized mice = 16.82---2.29; LD 4:20, sham-bulbectomized mice = 30.34 -+3.40; LD 16:8, sham-bulbectomized mice =
26.67---3.82). This effect of surgery disappeared 10 weeks after
bulbectomy.
405
6 WEEKSPOST-SURGERY
300
£
250
200
150
100
50
0 -
~
m
OBx
SHAM
OBx
LD 4:20
SHAM
LD 16:8
Epididymides
Paired epididymal mass was lower in olfactory bulbectomized
mice as compared to sham-operated animals after being housed for
6 weeks in short days 00<0.01) or long days 00<0.05) (Table 1).
However, epididymal mass was statistically equivalent between
short-day and long-day bulbectomized mice 00>0.05) (Table 1).
No photoperiodic effects on epididymal mass were evident in
bulbectomized mice examined 10 weeks after surgery 00>0.05)
(Table 1).
Mice that were injected with testosterone when three days old
and maintained from birth until 9 weeks of age in LD 4:20
photoperiods possessed smaller epididymides than short-day mice
injected with oil perinatally (p>0.05), or long-day animals regardless of injection treatment 00<0.05 in each case) (Table 1). There
were no photoperiodic effects on epididymal mass among mice
implanted with empty capsules or capsules containing testosterone
00>0.05 in all cases) (Table 1). There were no effects of
photoperiod on epididymal sperm numbers 00>0.05 in all instances).
Seminal Vesicles
All seminal vesicles were drained prior to weighing and
short-day mice subjected to olfactory bulbectomy or a sham
procedure possessed lighter seminal vesicles 6 weeks postsurgery
as compared to long-day animals 00<0.05) (Table 1). At 10 weeks
postsurgery, sham-operated long-day mice had heavier seminal
vesicles than short-day sham-operated mice or olfactory bulbectomized mice in either photoperiod 00<0.01) (Table 1).
Similarly, the seminal vesicles of long-day mice injected at 3
days of age with oil were heavier than those of oil-injected
short-day mice or seminal vesicles of testosterone-injected animals
in either photoperiod 00<0.001) (Table 1). There were no significant differences among the seminal vesicle weights of mice
bearing capsules (p>0.05) (Table 1).
10 WEEKSPOST-SURGERY
200
150
100
50
0
Oe,
SHAM
LO 4:20
Body mass did not differ significantly among any of the
experimental groups 00>0.05 in every case) (Table 2).
Olfactory-bulbectomizedmice had smaller epididymal fat pads
6 weeks postoperatively as compared to animals undergoing sham
operations 00<0.01) (Table 2); this effect of surgery disappeared
in animals assessed 10 weeks after surgery 00>0.01) (Table 2).
The epididymal fat depots were significantly heavier in shortday mice subjected to perinatal injections of oil as compared to
mice in all other experimental groups 00<0.01) (Table 2). Conversely, mice housed in LD 4:20 photoperiods and beating
testosterone-filled capsules had reduced epididymal fat stores as
compared to short-day mice with empty capsules or long-day mice
bearing empty or testosterone-filled capsules 00<0.05 in each
case) (Table 2).
SHAM
LO 16:B
9 WEEKSPOST-INJECTION
300.
250.. ¢
200.
tn
150,
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100.
50,
0
T
OiL
T
LD 4:20
OIL
LD 16:8
g WEEKSPOST-IMPLANTA'nON
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Body Mass and Epididymal Fat
OBx
~
1SO
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I
50,
T
E
LO 4:20
T
E
LO 16:8
FIG. 1. Mean paired testes mass ( ± S.E.M.) ofMus musculus (a) 6 weeks
after olfactory bulbectomy (OBx) or a sham-procedure (SHAM) and
maintainedeither in short (LD 4:20) or long (LD 16:8) photoperiods or (b)
10 weeks after surgery. Also depicted in this figure are mean paired testes
masses (_+S.E.M.) of house mice nine weeks after receivingan injection
either of testosterone (T) or sesame seed oil (OIL) (c) or implanted
subcutaneouslyeither with an empty Silastic capsule (E) or one filled with
testosterone (T) (d).
406
NELSON
TABLE 1
MEAN [_+ STANDARD ERROR OF THE MEAN (-+ S.E.M.)] PAIRED EPIDIDYMAL AND
SEMINAL VESICLE MASSES OF HOUSE MICE
Paired Epididymal
Mass (mg)
Seminal Vesicle
Mass (mg)
LD 4:20
LD 16:8
LD 4:20
LD 16:8
Olfactory bulbectomy
(6 weeks postsurgery)
63.9
± 1.5
n = 20
68.1
± 1.5
n = 22
64.4
± 2.3
n = 20
71.5
± 3.7
n - 22
Sham bulbectomy
(6 weeks postsurgery)
77.3
± 1.9
n = 22
73.2
± 1.3
n = 20
62.4
± 1.4
n = 22
75.4
_+ 1.5
n = 20
Olfactory bulbectomy
(10 weeks postsurgery)
78.1
_ 1.9
n = 20
76.1
+_ 1.8
n = 22
82.1
_+4.4
n = 20
79.6
_+2.8
n = 22
Sham bulbectomy
(10 weeks postsurgery)
77.6
_+2.6
n=22
85.1
_ 1.7
n=22
72.5
_+4.3
n=22
90.7
_+2.3
n=22
Testosterone
injection
65.2
+- 1.7
n=16
73.9
+_0.8
n=30
64.2
+_3.1
n=16
59.5
_+3.1
n=30
Oil injection
72.7
_+1.6
n=26
75.0
_+1.5
n=28
68.2
_+2.7
n=26
94.6
_+2.9
n=28
Testosterone
implant
72.9
-+ 1.3
n = 22
72.4
_+ 1.7
n = 22
78.5
_+2.7
n = 22
75.9
_+2.9
n = 22
Empty implant
80.3
_+ 1.9
n=20
77.2
_+2.0
n = 18
86.5
_+3.2
n=20
80.9
_+2.3
n = 18
DISCUSSION
The results of this study demonstrate that house mice can
discriminate day length, and thus indicate that the physiological
mechanisms underlying photoperiodism are extant in this " n o n photoperiodic" species. Short days delayed reproductive maturation of olfactory bulbectomized house mice, but not of neurologically
intact mice when examined six weeks after surgery. Ten weeks
postsurgery, the short-day bulbectomized mice appear to catch-up
developmentally with the other mice. Short-day mice that were
injected with testosterone when three days old had smaller gonads
nine weeks later as compared to long-day mice injected with
testosterone or mice injected with oil and maintained in either
photoperiod. These results are in agreement with the reproductive
effects of peripubertal olfactory bulbectomy and perinatal testosterone treatment in short-day rats.
However, peripubertal mice implanted with capsules containing testosterone did not respond to day length as did rats (24,25).
Mice implanted with capsules containing testosterone possessed
smaller testes than animals bearing empty capsules. Photoperiod
did not affect reproductive function in these mice. Capsules were
made proportionally smaller in mice than used for rats (24,25), but
apparently the estimated dose of testosterone was too high and
suppressed gonadal size. It is possible that any effects of photoperiod on the gonads were overridden by high levels of testosterone, and that smaller testosterone capsules may have permitted the
overt expression of a photoperiodically mediated response.
Essentially, sperm production was unaffected by photoperiod.
These results conform with the results of studies on rats in which
spermatogenesis and fertility were unaffected by photoperiod (16).
The lack of effect on sperm number strongly suggests that the
ability to discriminate long from short days probably plays no
functional role in the breeding of laboratory mice. Presumably,
reproduction of Mus has been uncoupled from photoperiod via
artificial and natural selection (5). Despite the apparent lack of
functional significance of photoperiodism in regulation of house
mice reproduction, the results of this study provide an existence
proof for the physiological mechanisms of photoperiodism.
Very short days were used in this study. Pilot data indicated
that olfactory-bulbectomized Mus were not responsive to LD 8:16
photoperiods, and only minimally responsive to LD 6:18 (Nelson,
unpublished data). An analogous situation exists in laboratory rats.
Bulbectomized male rats exhibited retarded gonadal growth in LD
8:16 photoperiods, but not when maintained in LD 10:14 photoperiods. Similarly, the critical photoperiod for rats bearing subcutaneous implants of testosterone was between 8 and 9 hours of
light per day (24). The necessity of very short photoperiods to
elicit photoperiodic responsiveness appears common to both laboratory rats and mice.
The manner by which olfactory bulbectomy and early testosterone treatment unmask photoperiodic responsiveness in mice is
unknown. Short-day exposure reduces prolactin levels in rats;
when short-day exposure is paired with an experimental manipu-
P H O T O P E R I O D I S M IN H O U S E MICE
407
TABLE 2
MEAN (-+ S.E.M.) BODY MASS AND EPIDIDYMAL FAT DEPOTS OF MALE
HOUSE MICE
Body Mass (g)
Paired Epididymal
Fat Depots (mg)
LD 4:20
LD 16:8
LD 4:20
LD 16:8
Olfactory bulbectomy
(6 weeks postsurgery)
27.57
-+0.68
n = 20
28.08
---0.74
n = 22
365.2
± 46.7
n = 20
413.2
---57.1
n = 22
Sham bulbectomy
(6 weeks postsurgery)
31.97
--+0.49
n=20
34.24
± 0.70
n=20
588.5
± 32.6
n=22
547.2
---43.6
n=20
Olfactory bulbectomy
(10 weeks postsurgery)
30.09
__+0.58
n = 20
29.36
±0.54
n = 22
519.1
---43.6
n = 20
448.6
+--46.5
n = 22
Sham bulbectomy
(10 weeks postsurgery)
29.76
--- 1.04
n=22
37.46
_ 0.69
n=22
498.0
± 68.6
n=22
547.0
+ 39.8
n=22
Testosterone
injection
32.11
± 0.50
n = 16
33.73
± 0.26
n = 30
570.8
---26.7
n = 16
426.5
---31.8
n = 30
Oil injection
32.17
___0.53
n=26
33.94
_ 0.36
n=28
734.7
± 32.3
n=26
497.9
± 24.0
n=28
Testosterone
implant
32.59
± 0.48
n=22
35.89
± 0.72
n=22
340.7
- 22.6
n=22
643.0
+ 79.3
n=22
Empty implant
33.79
±0.60
n=20
35.55
± 1.09
n=18
512.6
±35.8
n=20
542.9
±71.5
n=18
lation that reduces gonadotropin levels (e.g., testosterone treatment or bulbectomy), the resulting endocrine profile resembles
that o f a so-called photoperiodic species, that is, decreasing
circulating levels o f prolactin and gonadotropins (Nelson, Moffatt
and Goldman, unpublished data) (19). Depressed plasma levels o f
LH and increased or unaffected plasma prolactin levels were
observed in female blinded, bulbectomized rats (1,2).
The discovery that two archetypical " n o n p h o t o p e r i o d i c " rodent species, namely Mus musculus and Rattus norvegicus, can
discriminate day length raises questions about the usefulness o f the
terms " p h o t o p e r i o d i c " and " n o n p h o t o p e r i o d i c . " The ability to
measure day length may be tightly conserved over many taxa, but
the linking o f various physiological and behavioral processes to
photoperiodic regulation may vary widely a m o n g individuals
within a population. It seems reasonable to suggest that the ability
to discern the time o f the year may be a fundamental trait o f
animals and as advantageous as the ability to discern the time o f
day (6). Although reproduction appears to be uncoupled from
photoperiodic control in rats, house mice, and humans, the extent
to which nonreproductive traits are influenced by day length
remains largely unexamined.
ACKNOWLEDGEMENTS
I thank J. Rhyne-Grey, M. Kita, J. DiLeo, K. Perry, M. Chider and G.
Dales for excellent technical assistance. This research was supported by
NIH grant HD22201 and BRS grant S07RR07041 awarded by the
Biomedical Support Grant Program, Division of Research Resources.
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