Download Social Control of the Ovarian Cycle and the

AMER. ZOOL., 21:243-256 (1981)
Social Control of the Ovarian Cycle and the
Function of Estrous Synchrony1
MARTHA K. MCCLINTOCK
Department of Behavioral Sciences, The University of Chicago,
V
5730 Woodlaum Ave., Chicago, Illinois 60637
SYNOPSIS. The social signals among groups of females can either enhance or suppress
ovarian cyclicity. The ovarian cycle is not unitary, but is instead the integrated product of
several different components which are each affected by social signals of different modalities. This interaction between female behavior and ovarian cycle components has different manifestations in different species. Depending on its temporal context and the
social and physical environment, the same behavior/hormone interaction can take different forms. In some contexts, these interactions can be adaptive for the individual. In
others, they can generate a strong epiphenomenon or artifact that may not confer a direct
adaptive advantage itself, but still be necessary for other aspects of the coordination between social behavior and reproduction.
INTRODUCTION
ESTROUS SUPPRESSION
Successful reproduction, in a socially
breeding species, depends on an intricate
temporal coordination between social behavior and endocrine events. Males and
females must be fertile at the same time,
find each other, mate, and then produce
young in a physical and social environment
in which the offspring can survive. Utilizing information about the environment,
an individual female can minimize the loss
of fitness resulting from such mistimed reproductive events as unfertilized ovarian
cycles or pregnancies wasted through high
infant mortality. However, this coordination requires signals from her social and
physical environment which can be transduced by the brain and used to regulate
reproductive neuroendocrine function. In
addition, because her behavior mediates
her exposure to a complex array of social
signals and environmental stimuli, the reciprocal interaction between behavior and
hormones is essential to the temporal coordination underlying successful reproduction. This paper will focus on the behavioral regulation of ovarian cyclicity by
the social interactions among females, a
source of reproductive coordination that
has not been adequately examined.
Van der Lee and Boot (1956) provided
the first demonstration that female behavior could modify ovarian cyclicity. Female
mice (Mus musculus) living in small groups
mutually suppress each other's 4-day
cycles and become pseudopregnant, the
phenomenon since referred to as the LeeBoot Effect (van der Lee and Boot, 1956;
Lamond, 1959). The degree of estrous
suppression is dependent on the size of the
social group: females living in pairs do
continue to cycle, although irregularly,
while females living in large groups of thirty or more are completely anestrous (Whitten, 1959). Similarly, hamsters (Mesocricetus auratus) taken from an all-female group
are less likely to mate than are solitary females (Lisk et al., 1974; Brown and Lisk,
1978).
Against this background of ovarian
suppression, the odor of a male is sufficient to reinstate cyclicity across the group
of female mice (Whitten, 1958). All females respond simultaneously to the same
external signal from the male producing
an estrous synchrony within the group
known as the Whitten Effect. The induction of cyclicity by males is taxonomically
widespread among spontaneous and induced ovulators: birds (Streptopelia risoria)
(Lehrman, 1965); ungulates (sheep
1
From the Symposium on Social Signals—Compar- [Schinckel, 1954; Averill, 1955]; caribou
ative and Endocrine Aspects presented at the Annual [Rangifer tarandus] [Bergerus, 1974] and
Meeting of the American Society of Zoologists, 27pigs [Signoret, 1976]); reptiles (Anolis car30 December 1979, at Tampa, Florida.
243
244
MARTHA K. MCCLINTOCK
olinensis) (Crews, 1979); lagomorphs and nature of social control of ovarian cyclicity
soricid insectivores (Conaway, 1971); mi- by females and its function for the temcrotine rodents (Cross, 1972; Gray et ai, poral coordination of successful reproduc1974; Stehn and Richmond, 1975); and hu- tion.
man (McClintock, 1971; Cutler, 1980) and
nonhuman primates (Cercopithecus talapoin ESTROUS ENHANCEMENT AND SYNCHRONY^
[Rowell and Dixson, 1975]; Lemurf.fulvus
In both rats and humans, the effect of
[Harrington, 1975]; Macaca mulatto, [Con- an all-female social group on ovarian cyaway and Sade, 1965]). Such induction clicity is markedly different than in the
represents an efficient strategy for coor- mice and hamsters described above. The
dinating the fertile periods of males and ovarian cycles of females that live together
females. However, as the taxonomic dis- are enhanced rather than suppressed, and
tribution of female estrous suppression is also synchronize with each other (rat [Ratnot known, it may or may not be a neces- tus norvegicus; McClintock, 1978]; human
sary prerequisite for the estrous induction [McClintock, 1971; Russell, 1977; Quadby the male found in these species.
agno et al., 1979; Graham and McGrew,
Although the female suppression of the 1980]). This ovarian synchrony is different
Lee-Boot Effect is a robust phenomenon from the Whitten Effect because it results
in the laboratory, its adaptive significance from the continuous interactions of onis not obvious (Bronson, 1977; Rogers and going cycles within a female group rather
Beauchamp, 1977). In the field, as in the than from an external signal such as a male
laboratory, it may provide the background odor which simultaneously releases fenecessary for synchrony induction by the males from an acyclic condition.
male. If so, all-female groups should be
common, especially prior to the breeding Enhancement of ovarian cyclicity:
season. However, all-female groups are The effect of group living per se
only rarely encountered in wild Mus popGroup living enhances two aspects of rat
ulations (Frank, 1957; Crowcroft and ovarian cyclicity: the regularity of a cycle's
Rowe, 1963) and even then it seems im- length and the integration of the different
probable that females would not encoun- components of the estrous cycle. In
ter the male intruders or odor-trails that healthy laboratory rats the estrous cycle is
would prevent complete ovarian suppres- four (and occasionally five) days long (Nesion. Perhaps ovarian function evolved in quin etal., 1979). (Day 1 is called proestrus
the continuous presence of males and the followed by estrus, metestrus and diestrus
Lee-Boot Effect simply reflects a depen- I [plus diestrus II in a 5-day cycle].) This
dence on the male's presence for normal cycle length is determined by the repeated
ovarian function (Rogers and Beauchamp, coincidence of its anatomical, physiologi1977). However, the dose-dependent re- cal, and behavioral components whose colationship between the size of the female ordination is necessary for conception.
group and the degree of estrous suppres- Once every four days, the vaginal wall besion suggests a more specific role for the comes cornified; the uterus balloons and
female social environment.
then loses its retained fluid; estrogen and
It is undoubtedly precipitous to expect LH rise followed by ovulation; and the fea satisfactory functional explanation of an male comes into behavioral estrus showing
interaction when it may be only partially a lordosis reflex to flank stimulation, redescribed. The effect of female behavior ceptivity, and active solicitation of the male
on ovarian cyclicity has only been investi- (McClintock and Adler, 1978a). Each of
gated in a very limited number of species these cyclic components normally has a
and contexts, raising the possibility that 4-day period with peak levels coincidunder some conditions, female interac- ing within 24 hr (night of proestrus to the
tions might also enhance as well as sup- day of estrus).
press ovarian function. This, then, is the
Estrous cycle length: Mediation by olfactory
general problem that I will address: the signals. Female rats living in groups of five
245
SOCIAL CONTROL OF THE OVARIAN CYCLE
90
1
40
80
•
7
°
30
60
2
so
o
*
40
30
20
10
g
i o
4 Day
g i o
5 Day
g j o
Acyclic ( M =7days)
Group
FIG. 1. Social enhancement of ovarian cyclicity. The
percentage of experimental time (30 days) spent in
cyclic or acyclic state. Grouped female rats lived in
six groups of five each (n = 30). The solitary females
were either isolated (n = 30) or shared only olfactory
communication with four other solitary females
(eight groups, n = 40).
had more regular 4-day cycles than those
living alone (see Fig. 1). The cycles of
solitary rats were longer and more irregular. This difference confirms the finding
of Aron et al. (1971). Thus, in the rat, social interactions enhanced the regularity of
ovarian cyclicity, as indicated by changes
in vaginal cytology.
What are the social signals that mediate
this enhancement? When solitary females
shared a recirculated air supply with four
other solitary females, the number of regular 4-day cycles was comparable to those
living in a group (see McClintock, 1978,
for the equipment design which allowed
olfactory but prevented auditory communication). As communication between
these solitary females was airborne without
any physical contact with a substrate, these
results along with those of Aron (1973)
suggest that the primary olfactory system
rather than the vomeronasal system (Johns
et al., 1978) mediated the social signals
emitted by females which shortened and
regularized the ovarian cycle.
Solitary
• isolate
- olfactory
FIG. 2. Tonic lordosis in cycling solitary female rats.
The percentage of each vaginal cycle which was associated with a strong lordosis reflex to manual stimulation. The mean percentage ± SEM was calculated
for each cycle type found in females living under
three conditions: groups of five (six each, n = 30);
solitary isolates (n = 30) or shared olfactory communication among a group of 5 solitary females
(eight groups, n = 40).
Integration of ovarian cycle components: Ineffectiveness of olfactory signals. Social inter-
action among females affects the integration of ovarian cycle components as well as
their periodicity. Vaginal cornification and
the lordosis reflex normally appear together during the evening of proestrus. However, during social isolation, these components of the ovarian cycle no longer had
the same temporal pattern and were therefore dissociated from each other (see Fig.
2). In many solitary females, the lordosis
component was no longer cyclic. A lordosis
reflex could be elicited on any day even
though vaginal cornification continued to
appear only once every four or five days.
Thus the lordosis reflex occurred without
vaginal cornification. This tonic pattern in
the lordosis component has been reported
during acyclic periods of persistent vaginal
cornification. However, the fourfold increase in the lordosis component even dur-
246
MARTHA K. MCCLINTOCK
Estrous Synchrony
(Group size = 5 )
10
separate
together
8
•-
£
13
15
21
17
Days
=
23
25
27
29
31
33
Synchrony Threshold
FIG. 3. The development of estrous synchrony within a group of five female rats, after regrouping from the
colony. Estrous score: Lordosis reflex = 1 point. Cornified vaginal smear = 1 point. Highest possible group
total = 1 0 points. Synchrony threshold = 5 points. Scores above this value indicate that the majority of the
group is in estrus.
ing regular 4- and 5-day vaginal cycles represented a marked dissociation between
these normally tightly coordinated components.
What are the social signals that normally
maintain the integration of the vaginal and
lordosis components in females living in
groups? Surprisingly, in contrast with its
effect on the cycle length of the vaginal
component, a shared air supply did not
reinstate the lordosis pattern seen in
grouped females. Thus the cyclicity of the
lordosis component and its integration with
the vaginal component was not maintained
by olfactory communication. Our work in
progress indicates that neither auditory
nor visual communication is sufficient, nor
is the opportunity for exercise nor the lower temperatures found in the larger cages.
Preliminary results indicate that the normal pattern of the lordosis component
may depend on body contact with other
females. Whatever the social signals are, it
is now clear that the vaginal and lordosis
components of the ovarian cycle in the rat
are each maintained by social signals of
different modalities.
lordosis components were measured, the
estrous phases of the members of a group
begin to coincide two to three cycles after
the females were grouped together. That
is, the majority of the group came into estrus on a particular day and then again
repeatedly at 4-day intervals thereafter
(see Fig. 3).
Synchrony is a complex process depending on the interaction of particular members of a group, not on group living per se
(McClintock, 1978). While it has been
shown that airborne chemical signals are
sufficient to produce estrous synchrony
(McClintock, 1978), it is not yet known
whether synchrony is the result of signals
from a leader or zeitgeber within the group
or the interaction of equipotent signals
from several individuals. A coupled oscillator model of synchrony does suggest that
synchrony would require not only a mutual enhancement but a suppressive effect
or refractory period as well (von Hoist,
1969; Hoppensteadt and Keller, 1976).
Furthermore, an individual's hormonal
state or cycle phase should modulate the
olfactory signals that produce the enhancement and suppression that would result in estrous synchrony. The first eviEstrous synchrony
Group living also affects the coordina- dence along this line of inquiry was the
tion of ovarian cycles between individuals, demonstration that tonic odors from feresulting in synchronization of their es- males in light-induced persistent estrus (an
trous cycles. When both the vaginal and acyclic and pathological state) induced that
SOCIAL CONTROL OF THE OVARIAN CYCLE
247
same acyclic state in rats living downwind
but not upwind (McClintock and Adler,
19786). The next step has been to examine
the effect of tonic odors from females in
the normal phases of the estrous cycle
^jroestrus, estrus, metestrus and diestrus)
on the maintenance of synchrony within a
group. We have placed a group of female
rats (n = 6) with pre-established synchronized estrous cycles downwind from a tonic proestrous odor source (the phase during which ovulation and mating behavior
occurs; see Fig. 4, Group A). This tonic
odor source was created by rotating females that were expected to become proestrous through the odor source box each
day. The intensity of the tonic odor varied
with the availability of proestrous females
in the colony and with the accuracy of our
predictions. The tonic odors from proestrous females overrode the olfactory interactions of the group, desynchronizing
their estrous cycles. (Individual cycles were
maintained.) When the females creating
the tonic odor were in metestrus (the cycle
phase in which gonadotrophins are low),
the synchrony of the group reinstated itself. A second group, run simultaneously
with the first but in a reversed sequence,
replicated the effects (see Fig. 4, Group
B). Further, a desynchrony between group
members immediately followed a single
day-long pulse of proestrous odor in the
middle of a tonic metestrous stimulus (this
occurred in Group B on Day 16). The gap
of a single day in the tonic proestrous odor
was sufficient to reinstate a synchrony
(Days 31-36, Group B), only to have it dissipated once again when the tonic proestrous odor was reinstated. A gap in the
tonic metestrous odor did not have this
effect (Group A on Day 23). Thus, in conclusion, odors from females in the proestrous phase of the estrous cycle are very
likely one of the social signals that under-
FIG. 4. Estrous desynchrony by tonic odors from
proestrous females. The density of each square indicates the number of female rats in a particular estrous cycle phase (P = proestrus, E = estrus, M =
metestrus, D = diestrus). Thus a descending left-toright diagonal pattern reflects estrous synchrony. For
example, the diagonals seen across Days 1-4 for both
Groups A (n = 6) and B (n = 6) reflect their pre-established synchrony: The majority of each group was
in the same phase of the estrous cycle on the same
day. The number of animals in each odor source box
varied from 0 to 6. Experiments in wind tunnels A
and B were run concurrently.
248
MARTHA K. MCCLINTOCK
lie group synchrony, because they can
override or jam the signals among a synchronized group. This does not appear to
be so for odors from females in the metestrous phase of the cycle.
ADAPTIVE SIGNIFICANCE:
TEMPORAL CONTEXTS AND ARTIFACTS
Estrous and menstrual synchrony have
several troubling aspects from an adaptive
standpoint. First, synchrony usually requires that a stable group of females interact over three or more consecutive cycles
(McClintock, 1978). One would be hard
pressed to argue that this necessary condition is frequently found in the wild.
Many females would normally be pregnant, preventing the consecutive series of
cycles necessary for the development of
synchrony. In fact, in many species a menstrual or estrous cycle is relatively rare
because the majority of conceptions occur
in the context of a single postpartum estrus or result from the first or second ovulation of a season, starting an alternation
between pregnancy and lactation ([Conaway, 1971]; rats [Rattus norvegicus and Rattus rattus] [Steiniger, 1950]; talapoin monkey [Miopithecus talapoin] [Rowell, 1977]).
In other socially breeding species, pregnancy and lactation reduce the proportion
of time that a female spends cycling to a
small fraction, which also reduces the opportunity for the females of a group to
cycle concurrently (yellow baboon [Papio
cynocephalus] [Altmann et al., 1977]; human hunter-gatherers [McClintock, 1980]).
Even when many consecutive ovarian
cycles do occur in a group of females, such
as in the laboratory rat or among contracepting or celibate women, synchronization represents a proportionately small
shift in the timing of an individual's
cycle—1 or 2 days in the rat and 3 or 4
days in the human. What, then, is its function? Or, does it have a function?
Not all easily observable or consistent
traits have a selective advantage or have
served a function. It may well be that the
behavior/hormone interactions which consistently modify and synchronize ovarian
cyclicity in the laboratory environment are
interactions which evolved because of their
manifestations occurring under a different
variety of social and physical environments
and at different times in the reproductive
life span. This line of reasoning then suggests that a functional discussion of synchrony should not only consider the funcA
tion of the phenomenon as it was originally
observed but should also explore the alternative forms or manifestations of its underlying mechanisms.
The following discussion will serve two
purposes. First, by drawing on the comparative literature it will generate testable
hypotheses about the possible manifestations, adaptive significance and evolution
of the particular behavior/hormone interactions described above which produce
ovarian enhancement and synchrony in
Rattus norvegicus. Second, it will serve a
more general and comparative purpose by
outlining different phenomena that similar interactions might produce in the
widely varying social and physical environments of different species. In other words
it will suggest data analysis strategies for
species in which the absence of consecutive
cycles or stable female groups precludes
the emergence of synchrony, but in which
the behavioral control of ovarian cyclicity
may still be integral to successful reproduction. The discussion will be organized
around four temporal contexts of reproductive function: the life span, seasons, the
birth cycle and the ovarian cycle (see Fig.
5).
The life span
During her life span, a female rat moves
from a prepubescent anestrous state to a
cyclic adult reproductive pattern and then
into reproductive senescence. If the reproductive condition of the adult females in
a group is a good indicator that the environment is suitable for reproduction, the
prepubertal female could use this information in her social environment to make
the energy investment necessary to attain
maturity and start cycling. In the context
of the life span, the behavior/hormone interactions which produce estrous enhancement and synchrony would be manifested
by changes in the rate of maturation or by
synchrony at menarche. Similarly, when
LIFESPAN
POSSIBLE FORMS
Change in rate of
maturation 8 aging
Prepubertol
Anestrus
SEASON
Lower variance in
Seasonal
breeding 8 birth peaks
Anestrus
BIRTH CYCLE
Implantation^!
Pregnancy
B i
| //Birth
Altered time of implantation
or return to cyclicity
Lactation
OVARIAN CYCLE
\ r\
Anestrus
J
^
\J
Acyclicity
s\
\J
r\
\J
r\
\
Coupled cycle phases
or endocrine states
Fie. 5. Temporal contexts for the behavioral control of ovarian cyclicity. The behavior-hormone interactions which produce estrous synchrony may
be manifested by other phenomena in different temporal contexts.
250
MARTHA K. MCCLINTOCK
the environment can support a reproductive state in the young mature females of
a burrow, an older female could use this
information as a basis for extending her
reproductive life span and slowing the rate
of senescence.
Social interactions between females delay menarche in laboratory populations of
rodents which also show estrous suppression, i.e., the Lee-Boot Effect (Mus musculus, Christian, 1971; Vandenbergh, 1969)
as well as in female groups of Peromyscus
maniculatus bairdii (Terman, 1968); Peromyscus leucopus (Rogers and Beauchamp,
1976) and marmosets (Callithricidae [Epple, 1973]). It has been hypothesized that
this female-female suppression during puberty confers a selective advantage (Mus
musculus [Vandenbergh, 1975]; Peromyscus
leucopus [Rogers and Beauchamp, 1976])
in that it may postpone the attainment of
puberty in dispersing populations or under social conditions in which fertile males
are scarce (Bronson, 1979).
serve several different functions within the
same species. Among the bank swallows
mentioned above, information about an
abundant but ephemeral food resource is
integrated through social foraging patterns of a colony. Fledglings born in ttm
middle of a birth peak that can utilize this
social information source have a more efficient foraging pattern, and consequently
a higher survival rate, than those born late
in the season that must forage without
adults or alone (Emlen and Demong,
1975). In vervets (Cercopithecus aethiops), in-
fants born late in the season may also suffer nutritional deprivation (Klein, 1978).
The incidence of cub killing in lions
(Panthera leo L.) is reduced when births are
synchronized within a pride (Bertram,
1975). Likewise, cannibalism is reduced
during the breeding peaks of carrion
crows (Corvus corone [Yom-Tov, 1975]),
and fewer clutches are lost to intergroup
aggression when colonies of the Peruvian
booby (Sula variegata) and red-footed booby (Sula sula) exhibit local breeding synSeasons
chrony (Nelson, 1970). All of these examThe adaptive significance of birth syn- ples may reflect the loss of fitness incurred
chrony and seasonality has recently been by raising young ahead of the peak when
well established in a variety of species, doc- territories and mate choice are still in disumenting a selection pressure for mecha- pute (Drickamer, 1974; Hrdy, 1974).
nisms that would produce birth synchrony. Those vervets born late in the season may
Among bank swallows (Riparia riparia), not receive the attention and social advanbirth position relative to the birth peak ac- tages of those born earlier (Lancaster,
counted for 68% of the variance in repro- 1971).
ductive success. Direct measurements indiBirth synchrony can also confer an
cated that vulnerability to predation was adaptive advantage at several points in the
reduced during the breeding peak (Emlen life span. Green turtles (Chelonia mydas)
and Demong, 1975). Similar effects have must hatch in synchrony with nestmates in
been demonstrated in Black-headed gulls order to dig upwards as a group to reach
(Lars ridibundus) (Patterson, 1965). Pre- the sand's surface. Later on, synchrony besumably a birth peak "swamps" the exist- tween broods reduces the percentage lost
ing predator population, whereas the to predation as the turtles migrate to the
smaller number of eggs in an off-peak lay- sea (Carr and Ogren, 1960).
ing allows the predator to take a larger
Breeding synchrony of a group involves
percentage. In addition to this supply-and- both temporal and spatial proximity of redemand model, it appears that defensive productive events. Darling's (1938) origimobbing is more effective during a peak nal hypothesis emphasized the advantage
laying period because of local social facili- of spatial proximity and increased group
tation (Kruuk, 1964). These anti-predator size which can result from synchronous
functions have also been suggested for breeding. However, more recent detailed
breeding synchrony in the wildebeest analyses based on direct measurements
(Connochaetes taurinus [Estes, 1966]).
have demonstrated that the adaptive adSynchronous breeding may ultimately vantage is conferred through the temporal
SOCIAL CONTROL OF THE OVARIAN CYCLE
coordination of reproductive events which
is generated by synchrony rather than by
spatial proximity (Yom-Tov, 1975).
What, then, are the proximate mechanisms of a temporal birth synchrony? In
0Mnales, the seasonal transition from a nonreproductive to a reproductive condition
of cyclic spontaneous ovulation can result
in synchronized matings and, in species
with low variability in gestation length,
synchronized births. This transition can be
brought about both by environmental factors and by the social interactions of a
breeding group. Sadleir (1969) and Fraser
(1967) have reviewed the wide variety of
environmental conditions that can bring
females from a nonreproductive to a reproductive state. Species will differ in the
strength of their response to such factors
as day length, rainfall, and temperature.
Some of these control mechanisms may be
synergistic: Changes in both day length
and temperature are necessary for the
breeding synchrony reported in lemurs
(Lemur f. fulvus [van Horn, 1975]). In addition to the macro-environment, changes
in the micro-habitat of the species may also
facilitate a reproductive state. Estes (1966)
has postulated that the dramatic breeding
synchrony of the wildebeest is generated
by an increase in their diet of new plant
growth which contains estrus-inducing
phytoestrogens (Shutt, 1966).
All of these mechanisms produce breeding synchrony through the simultaneous
response of each individual female to the
same environmental event. In addition, it
is possible that behavioral interactions
within the breeding group also produce
synchrony. This behavioral influence is
most salient in species that do not show
seasonal variations in breeding. The females within a pride of lions (Bertram,
1975), or within a harem of hamadryas
baboons (Papio anubis [Kummer, 1968;
Abbegler, 1976]) breed synchronously,
while there is no synchrony across the
prides of a region or across the baboon
troop as a whole. The clutches of small
groups of swallow tail gulls (Larus fucatus
[Hailman, 1964]) and North Atlantic gannets (Sula vassana [Nelson, 1970]) are locally synchronous, while the overall pat-
251
social * environmental cues
environmental cues alone
FIG. 6. Social signals can sharpen a breeding peak
produced by an environmental stimulus.
tern of an island colony of either species
is asynchronous.
When the signals generating breeding
synchrony are external, synchrony is externally generated, and social interactions
may sharpen a broad and less precise peak
created by the response to the external
variable (see Fig. 6). For example, synchronous breeding in groups of domestic
animals is often produced artificially (cows
[Britt et al, 1972]; pigs [Signoret, 1976];
hamsters [Gross, 1977]). In the dairy cow,
injections of prostaglandin produce a
broad estrous synchrony within the herd
(Cooper and Furr, 1974). When a herd
was also exposed to a mixture of cervical
mucus and urine from estrous cows, the
variance in estrous onset was significantly
reduced (Izard and Vandenbergh, 1979).
In many species, the social mechanisms
of breeding synchrony have not yet been
specified (Jay, 1965; Sugiyama et al., 1965;
Yoshiba, 1968; Hopf, 1972). In some, it is
undoubtedly interactions with a fertile
male that produce the synchrony (Sinclair,
1950; Schinckel, 1954; Whitten, 1958;
Conaway and Wright, 1962; Baldwin,
1970; Williamson et al., 1972). However,
interactions between females could also induce cyclicity and synchrony at the beginning of a breeding season.
For example, the Norway rat (Rattus norvegicus) is a seasonal breeder (Barnett and
Spencer, 1950; Steiniger, 1950; Davis,
1951; Leslie etal, 1951; Telle, 1966). This
seasonality depends on variations in nutrition (Cooper and Hayes, 1967), day length
(Hoffman, 1973), and temperature (Her-
252
MARTHA K. MCCLINTOCK
oux et al., 1959). Furthermore, the spon- tegrated by the social interactions of the
taneous ovulatory cycle of the wild strain group.
is probably closer in length to two weeks
than the 4-day cycle of the laboratory The birth cycle
strain (Long and Evans, 1922; Calhoun,
In species that show no clear seasonality
1962; McClintock and Adler, 1978a). A fe- or seldom have consecutive estrous cycles^
male that is more responsive to environ- the social control of cyclicity may be manmental cues would be the first to become ifest within the context of the birth cycle.
fertile and cycle at the beginning of a sea- The timing of several events during this
son. Other females could respond to this time span could be modified by the female
information via the behavior/hormone social environment: implantation; birth;
mechanisms described in the first half of and the return to cyclicity after parturithis paper. Not only could the initial fe- tion, lactation, or the loss of an infant. In
male affect the other females in her bur- cattle, an early postpartum cyclicity is afrow, but also those females with whom she fected by social signals from the herd (Frais in olfactory communication through ser, 1968). In langurs (Presbytis entellus
vaginal marking and urine deposits. If [Hrdy, 1977]) and yellow baboons (Altthere are only a few individuals that are mann et al., 1978) females resume cyclicity
ready to respond to such a social signal around the time that their infants are
with cyclicity (i.e., if only a few are in a weaned. As this interval is variable it could
sub-threshold condition [Cooper and potentially be modified by the females' soHayes, 1967; Rogers and Schwartz, 1976; cial environment as their lactational amenHarlan and Gorski, 1978]) then cycling in- orrhea ends. Thus, in this temporal condividuals may drop back into an anestrous text, the behavior/hormone interactions
state, especially if the environmental underlying ovarian enhancement and synevents which induced their cyclicity are chrony could in principle be manifested by
transitory. Such sub-threshold conditions alterations in the time of implantation,
are similar to the "silent heat" or "silent birth or the pattern of postpartum fertility.
ovulation" seen early in the breeding sea- This would affect the synchrony of births
son in sheep (Robinson, 1950; Averill, and parental care discussed above.
1955; Thibault et al, 1966); bank voles
{Clethrionomys glareolus S.), hedgehogs (Er- The ovarian cycle
inaceus europaeus L.) and elephants (LoxoSome species do reproduce under social
donta africanus B.) (Perry and Rowlands,
and
physical conditions which allow sev1962); cattle and horses (Fraser, 1968);
eral
consecutive ovarian cycles and the
sows (Pomeroy, 1960); and rabbits (Bramemergence
of synchrony. Estrous synbell, 1944). However, when a critical numchrony
may
have an adaptive advantage
ber of females begin to cycle, they may
itself,
especially
in species like the lion
mutually enhance and support each oth(Panthera
leo
L.)
where
only 20% of estrous
er's reproductive state and induce cyclicity
matings
result
in
a
pregnancy
(Bertram,
throughout the rest of the colony. If the
1975).
With
synchronization,
subordinate
presence of cycling females in a group is
a good indicator that the environment is males have the opportunity to mate and
suitable for reproduction, females may use monopolization by a dominant male is resocial interactions for information about duced. In the lion and yellow baboon, this
the environment. Further, these social sig- can reduce competition among males, and
nals would produce an information aver- promote social stability (Bertram, 1975;
aging effect that would minimize the spa- Hausfater, 1975). The group mating protial and temporal variations in an duced by estrous synchrony increases male
individual's immediate environment. Each sexual activity (cattle [Williamson et al.,
individual would in turn benefit by this 1972]) and could increase the parental insource of environmental information, in- vestment of males (Knowlton, 1979).
The mechanisms of synchrony not only
SOCIAL CONTROL OF THE OVARIAN CYCLE
253
include an enhancement of cydicity, but ual performance (Bedford, 1978; Campalso a suppressive effect or refractory pe- bell and Swanson, 1979). In addition,
riod (von Hoist, 1969). In some cases syn- group mating reduces the constraints imchrony may be generated by a leader or posed by the compromise inherent in pairzeitgeber that temporarily suppresses the wise mating, and each individual is freer
Cycles of other females. In lemurs, the to mate in a temporal pattern which endominant female of a group mates first sures pregnancy (McClintock et al., 1979).
while the mating of the remainder is deIn humans, menstrual synchrony has
layed (Harrington, 1975). The reproduc- different consequences. The phenomenon
tive rate of dominant female gelada ba- was culturally recognized by the religious
boons (Theropithecus gelada) is higher than belief system of the Yurok Indians, an abthat of subordinates (Dunbar and Dunbar, original group who lived along the Klam1977). A reinterpretation of the Lee-Boot ath River in northern California (Buckley,
Effect might reveal a similar system: As 1979). In this culture, sexual activity and
suppression is rarely found in all females conceptions were limited during the year
of the group, it could be that those who so that a significant proportion of the
remain cyclic are dominant, and, in mice, young women of the village did have sevcompletely suppress rather than just delay eral consecutive and unfertilized menthe cycles of the rest of the group (as strual cycles. For ten days following the
would occur in species that demonstrate onset of menstruation, Yurok women ensynchrony). Such an interpretation of the tered a menstrual hut, shed their daily reproximate mechanism of synchrony em- sponsibilities, had their meals prepared for
phasizes that the phenomenon evolved as them by other women, and focused on a
a result of the balance of separate func- personal quest for spiritual power. Furtions: for example, the dominant female ther, synchronously menstruating women
would be the first to mate with the avail- played central roles in Yurok historical
able males, while the remainder would narratives (Spott and Kroeber, 1942).
benefit from the facilitation of group mat- Women who were out of synchrony were
ing (Williamson et al., 1972; Bertram, advised to "talk to the moon" in order to
1975).
reinstate their cyclicity and position in the
menstrual group. Among the Karok, a
neighboring and related culture, the stelCAUSE AND CONSEQUENCES
Even though ovarian synchrony may not lar constellation which we call the Pleides
have a direct adaptive advantage, it may represented seven synchronized menstill occur regularly given the right social struating sisters (Harrington, 1931).
and environmental conditions. If so, other
These examples reflect the intricate insystems may utilize the- phenomenon, terdependencies of complex systems. Rats
which is itself an artifact or epiphenome- can reproduce successfully without synnon in evolutionary terms. For example, chronous estrous cycles and menstrual
neither the wild nor the laboratory strain synchrony in humans did not evolve beof Rattus norvegicus is monogamous. Rats cause of its cultural consequences. Howcan reproduce in groups in which several ever, the mating system of the rat and the
males and several females are mating at belief system of the Yurok Indians can
the same time. Thus, when estrous syn- each utilize a phenomenon that may conchrony does occur among the females of fer its adaptive advantage in another cona burrow (Steiniger, 1950) or breeding text.
cage (Charles River Laboratories: Wilmington, Mass.) the hormone/behavior inACKNOWLEDGMENTS
teractions of estrous synchrony will have
The author's research was supported by
set the social context for group mating. NSF BNS 78-03658 and institutional funds
Under group conditions, the presence of from Biomedical Research Grant PHS
several estrous females facilitates male sex- SOR-RR-07029 and The Spencer Foun-
254
MARTHA K. MCCLINTOCK
dation. The assistance of Mr. Stephen
Cogswell is gratefully acknowledged.
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