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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. 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