Photoperiodic Stimulation of Pubertal Development ... - Oxford Journals

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Jul 23, 1982 - in Male Deer Mice: Involvement of the Circadian. System. J. MAL. WHITSETT,'. HERBERT. UNDERWOOD and JAMES. CHERRY. Department.
OF REPRODUCTION

BIOLOGY

Photoperiodic

28,

652-656

(1983)

Stimulation

of Pubertal

Involvement J. MAL

WHITSETT,’

of the Circadian

HERBERT

North

Development

Raleigh,

System and JAMES

UNDERWOOD

Department Carolina

in Male Deer Mice:

CHERRY

of Zoology State University

North

Carolina

27650

ABSTRACT prairie deer mice (Peromyscus maniculatus bairdii) is accelerated by exposure of juveniles to a long-day photoperiod, and, conversely, retarded by exposure to short days. The purpose of the present study was to evaluate the possible involvement of the circadian system in the photoperiodic regulation of puberty. Weanling males, previously housed on a short-day light cycle of 6L:18D, were subjected to a “resonance” protocol in which they received one of the following light cycles: 6L:18D, 6L:30D, 6L:42D, 6L:54D, or 16L:8D. Postweaning exposure to cycles of 16L:8D, 6L:30D, and 6L:54D stimulated reproductive organ growth as measured at 6 weeks of age. Exposure to cycles of 6L:18D and 6L:42D failed to stimulate reproductive development. These data support the hypothesis that young male deer mice use a circadian rhythm of responsiveness to light to measure photoperiodic time and, consequently, regulate pubertal development. Pubertal

development

in

INTRODUCTION

Day length or photoperiod lished as an important factor in of seasonal cycles of reproduction of many species of vertebrates fishes (de Vlaming, 1972) (Boissin-Agasse et al., 1982)

is well estab the regulation in adults ranging from to carnivores and ungulates (Karsch et a!., 1980) among the mammals. Although less is known of the control of the initial transition from immaturity to a breeding state during puberty, recent evidence indicates that day length can influence pubertal development in several species of mammals including sheep (Foster, 1981), Djungarian hamsters (Hoffmann, 1981), voles (Grocock, 1981), white-footed mice (Johnston and Zucker,

1980;

and

prairie

1982; A

Whitsett central

periodism time general of

an

first,

Petterborg

deer issue the

nature

measurement. hypotheses

of

to as

the

measure

accumulates

proposed

measurement sumes a light. gered in the other 1971)

circadian sensitivity;

-

day

length.

day

or

Thus, a photoperiodic by the presence of circadian cycle, times. Pittendrigh emphasized the

light but

rhythm second,

not and

dual

response at certain by Minis role of

Zoology, Raleigh,

November 18, 1982. July 23, 1982. requests: 3. Mal

North Carolina NC 27650.

State

Whitsett, University,

is

trigtimes

light at (1964, light in

system: first, light for the organism’s including the

of photoperiodic photo light is photoperiodically

The

hypothesis,

-

Accepted Received 1Reprint

night.

amount of the then triggers the photoperiodic The second hypothesis, originally by Bunning (1936) to explain the of photoperiod in plants, ascircadian rhythm in sensitivity to critical

inductive only if the rhythm of photoperiodic photosensitivity is entrained in such a way that the photosensitive portion of the rhythm is illuminated. This kind of circadian mechanism has been termed the “external coincidence” model because it demands the coincidence of an external stimulus light with an internal rhythm of photosensitivity. More recently, Pittendrigh (1972) has propounded an “internal coincidence” model in which the internal coincidence of two or more

there are two for the ability

“hourglass”

the

a

kind of photoperiodic as an entraining agent many circadian rhythms,

Miller,

of photo

of

this acts

1980),

and

throughout

Accumulation product response.

photoperiodic

Currently, to account

organism known

Reiter,

mice (Whitsett Lawton, 1982). in the physiology

and is

and

holds that an organism does, quite literally, measure the length of the light (or dark) period. Presumably, some reaction product

-

Dept. of Box 5577,

652

-

-

SYSTEM

CIRCADIAN

24

PUBERTY

___

94

___

___________ ___________

0

653

72

___

___

00%

AND

___

___________

6 LIeD 6

each

EJ

L300

6L.42D

LJ

6L540

EEJ

FIG. 1. A hypothetical cycle (i.e., h 0-12,

night”

or photosensitive

circadian not

oscillators

induction

in

the

coincidence position, the

correct

phase

however, researchers in experimentally internal of

and

external

was

young

deer

to we

measure determined

to

several

day the ahemeral

This “resonance” in Fig. 1, involves (6 h) tervals

pulses such

the uses

(non-24 protocol, exposing

of light spaced that, for some

or light

To

date,

been successful between the mechanism during of this that the system

accomplish of juvenile h)

light

this, males cycles.

which is depicted deer mice to short at different individuals,

inthe

pulse recurs with a period of 24 h or a multiple thereof, and for other individuals, the pulse recurs with a period that is 12 h more (or less) than a multiple of 24 h. The former condition results in pulses always occurring during the

individual’s “subjective day,” whereas in the latter condition, one pulse falls during the subjective day and the alternating pulse falls during the “subjective night.” Assuming that a photosensitive phase of a circadian rhythm of photoperiodic photosensitivity occurs during the subjective night of an individual, light cycles of 6L:18D and 6L:42D should not stimulate development, but cycles of 6L:30D and 6L: 54D should be stimulatory. Light will fall in the light-sensitive portion of the circadian day every 3 or 5 calendar days for individuals on the 6L:30D and 6L:54D schedules, respectively. This general protocol has been used repeatedly in investigations of photoperiodic time measuring systems

photosensitivity and the remainder

day”

in adult mammals 1972; Grocock and deer

Enright, mouse

accordance no treatment should

of

models.

The purpose hypothesis its circadian

length. To response

photoperiodic

“subjective

is simply oscillators

is known of the time measurement

mouse

of

relationship.

coincidence

development. to test

study

of

whether role

system internal

have not discriminating

As yet, nothing photoperiodic

pubertal

determines occur. The

will

in an internal to entrain, or

circadian rhythm 24-36, etc.) is the phase of an individual.

light

in deer

in deer

and and

cycle

birds Clarke,

The first half of the “subjective

(Elliott 1974;

with

the involving

et al., Hamner

If the

1967; Turek, 1974). measures photoperiodic

young time in

hourglass hypothesis, 6-h pulses of light

stimulate development, because 6 are less than the critical photoperiod mice (Whitsett et a!., in preparation).

MATERIALS

AND

Prairie deer mice bairdii) were maintained polypropylene cages on

They

mice.

of the

were provided

METHODS

(Peromyscus in 28.5 X a

with

Blox

h

18.5

maniculatus X 12.0 cm

bedding of shredded aspen. tap water and Wayne F -6 Blox (during pregnancy

and Wayne Breeder lactation) ad lib. Adult male and female deer mice, housed previously on a light:dark cycle of 15L:9D, were paired for breeding in a room having a cycle of 6L:18D. Males were removed from the cages 5 days later. Females and offspring remained on the 6L:18D schedule until weaning. Male offspring were weaned at 20-2 3 days of age. Between 21 and 24 days of age, they were moved to a separate research facility where they were assigned, on a random basis, to one of 10 light-tight wooden chambers. Each chamber, measuring 1.21 X 0.45 X 0.61 m, was lighted by one fluorescent bulb controlled by a timer. The 30-W bulb (Sylvania F30T12 -CW-RS) produced an average intensity of 1100 lux at the level of the deer mice. Fresh

and

air

was

continuously.

the

supplied

Lights

by

were

a

ventilation

off

in the

fan

room

that

ran

in which

chambers were located. Each chamber, which held 9 cages of individuallyhoused deer mice, received one of the following treatments: 6L:18D, 6L:30D, 6L:42D, 6L:54D or 16L:8D. There were two replicate chambers per experimental treatment condition; thus 18 males received each treatment. Only males weighing between 8.4 and 10.9 g at weaning were used in the study. Light:dark cycles with a period of 24 h were controlled by electromechanical timers; ahemeral cycles were controlled by programmable electronic timers. On the first day of the treatments, lights were activated at 0600 h, the time at which the

654

WHITSETT

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FIG.

2. Influence

6:18

630

6:42

654

of light:dark

cycles

LD

168

on reproductive

extension of bar represents median and right extension group is significantly different from 6L:18D control, 16L:8D control (Duncan’s multiple range test, o=0.05).

males

had

experienced

the

Consequently, introduction chambers occurred during The

onset the

into light

of

light

the period.

since

birth.

photoperiod

males

remained in the chambers from 3 until 6 weeks of age, at which time they were removed, killed, and frozen at -20#{176}C. At a later date the deer mice were thawed and weighed. The area of the androgen -dependent ventral sebaceous gland (Doty and Kart, 1972) was measured, and testes and seminal vesicles were removed and weighed (Lawton and Whitsett, 1979). The design of the experiment was a single classification analysis of variance. The F tests were calculated using the General Linear Models procedure of the SAS computer program (Helwig and Council, 1979). As the distributions of responses to the various light cycles were sometimes highly skewed, results have been described by both means and medians in Fig. 2. This permits a simple evaluation of the direction and degree of skew and substitutes partially

for standard errors, which have little meaning for the highly skewed distributions. Prior to the calculation of F tests, a logarithmic transformation was applied to the data for testis and seminal vesicle weights. RESULTS

As ment

illustrated influenced

in Fig. 2, photoperiod reproductive organ

treatgrowth

618

630

642

6:8

6:54

organs in male deer mice at 6 weeks of age. Left represents mean. An asterisk (‘) indicates that treatment a pound sign (4fr) that it is significantly different from Sample size=18 per treatment group.

(testes,

F

vesicles,

F (4,85)2055,

gland, general 2.28,

(4,85)15.04,

P