Current Anthropology Volume 40, Number 3, June 1999  1999 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved 0011-3204/99/4003-0001 $2.50

The rich literature on the sexual behaviour of the Ho- mininae (Australopithecus and Homo) emphasizes the Loss of Oestrus and uniqueness in this regard of Homo sapiens and attri- butes considerable importance to the role of sexual be- haviour in the process of hominization and even in the Concealed evolutionary success of the species (e.g., Morris 1967, Alexander and Noonan 1979, Lovejoy 1981, Kourtovik in Evolution 1983, Parker 1987, Turke 1988). The absence of signs of ovulation and the accompanying so-called constant receptivity in human females are considered fundamen- tal. The uniqueness of their emergence in the evolution The Case against the Sexual- of the Hominoidea is assumed on the basis of the chim- panzee model. This assumption has produced many Selection Hypothesis hypotheses as to the evolutionary causes of various forms of sexual signaling and behaviour allegedly char- acteristic of the Plio/Pleistocene evolution of the Ho- by Bogusław Pawłowski mininae. The adaptive advantage of constant receptiv- ity has been suggested to be greater cooperation within the group and reduction of competitiveness among males (Etkin 1963, Pfeiffer 1969, Fox 1972, Daniels 1983), the emergence of (Etkin 1954, Morris The assumption that absence of oestrus and of manifestations of 1967, Lovejoy 1981), the intensification of paternal be- ovulation is specific to has given rise to various propos- als of a role for selection pressures in the evolution of these fea- haviour (Alexander and Noonan 1979; Symons 1979; tures in the form of sexual selection or other behavioural adapta- Strassmann 1981; Turke 1984, 1988), the possibility of tions. Analysis of the sexual behaviour of nonhuman primates acquiring greater quantities of protein through males’ and humans indicates, however, that constant receptivity is not hunting (Symons 1979, Hill 1982, Parker 1987), and the unique to humans and that human sexual behaviour is not inde- possibility of deceiving males as to their paternity (Ben- pendent of the phases of the . Quantitative differ- ences in the distribution of sexual behaviour between humans shoof and Thornhill 1979) and thus reducing the risk of and the nonhuman primates in question may be the result of on the part of males (Hrdy 1981). Other many morphological, ecological, and cultural factors of which hypotheses include the concealment of ovulation from those differences are side effects. In the case of the postulated se- the female herself, supposedly to increase the effective- lection pressures on the disappearance of visual manifestations of ovulation, the rather unlikely model of anogenital ness of deceiving males about females’ fertility (Alexan- swelling in the early Hominidae may be replaced by an early- der and Noonan 1979), and, in an improbable scenario hominoidal model in which the swelling was relatively small. Its advanced by Burley (1979), females’ conscious avoid- reduction in anthropogenesis may have been caused by bipedal lo- ance of the pain of childbirth by avoiding sexual con- comotion, the cost of water accumulation, hyperaemia of the tacts in the fertile, symptomatic phases of the men- area, and an increase in adipose tissue. Furthermore, olfactory communication in the context of sexual behaviour in the cli- strual cycle, with selection favoring females who were matic conditions of the African savannah would have been suffi- unaware of the moment of ovulation and therefore un- cient for detection of the fertile periods of the menstrual cycle. able to avoid pregnancy. Still other hypotheses have Thus, assuming the existence of direct selection pressures on sex- treated the loss of oestrus as a side effect of, for exam- ual behaviour in the Plio/Pleistocene evolution of the Homini- nae seems unjustified. ple, the increase in androgen levels associated with en- durance in walking and the pursuit of prey (Spuhler bogusław pawłowski is a Lecturer in the Department of An- 1979) or of the lengthening of the period of female re- thropology of the University of Wrocław (ul. Kuz´nicza 35, 50-138 sponsiveness in response to longer lactation (Kourtovik Wrocław, Poland). Born in 1962, he was educated at the Techni- 1983). cal University of Wrocław (M.Sc., 1986) and the University of The majority of hypotheses, however, assume the ex- Wrocław (M.Sc., 1989; Ph.D., 1996). His research interests in- istence of sexual selection pressure for behavioural clude the mechanisms of and human mate- choice strategies. His publications include (with R. Dunbar) ‘‘Im- change. These can be criticized not only in terms of pact of Market Value on Human Decisions’’ (Pro- comparative data on the detailed level but also in terms ceedings of the Royal Society, London, B 266:281–85) and ‘‘With- of the mechanisms of behavioural selection proposed— holding Age as Putative Deception in Mate Search Tactics’’ many of which postulate the existence of behavioural (Evolution and Human Behavior, 20:53–69) and (with A. Nobis) ‘‘Threat Making Cooperation, or How to Increase the Probability rules that if valid should apply to other animals (espe- of Cooperation in the Prisoner’s Dilemma’’ (Systems 3:112–19). cially nonhuman primates) as well. I shall concentrate The present paper was submitted 28 iv 98 and accepted 8 vii 98. here on questioning the correctness of the assumption that absence of oestrus and concealed ovulation in Homo are exceptional and showing that there are many environmental and cultural factors that may have in- fluenced the forms of sexual signaling and behaviour in human evolution.

257 258 current anthropology Volume 40, Number 3, June 1999

Loss of Oestrus as an Evolutionary Trend in males occurs in the proliferative and ovulatory phases Primates (Saayman 1970, Nadler 1981, Nadler et al. 1986, cited by Wallis and Englander-Golden 1992). A similar pat- tern is found in the initiative of males, for which visual, Oestrus is a period of strong sexual drive in the female olfactory, and behavioural signs in females constitute cycle in which the female accepts male copulation. It is changes in their attractiveness. Research on human sex- very clearly marked in, for example, rodents, carni- ual behaviour has demonstrated fluctuations in procep- vores, and lemuroids. Because in many primates, de- tivity and attractiveness approximating those in the spite the intensification of copulation in the ovulatory chimpanzee. Proceptivity in a woman is measured in phase of the cycle, females also allow males to copulate terms of such criteria as sexual self-excitement, initia- in other phases, Chalmers (1979), Loy (1987, cited by tion of hetero- and homosexual behaviour, sexual fanta- Wallis and Englander-Golden 1992), and Martin (1990, sizing and thinking, sexual desire, and number of or- 1992), among others, have maintained that oestrus does gasms (table 1). Despite the fact that these studies were not occur in this order. If so, its absence in humans may conducted among women from highly civilized cul- differ from the situation of many other primates in de- tures, the results indicate the dependence of proceptiv- gree rather than in kind. Detailed analysis of the differ- ity on the phases of the menstrual cycle much as in the ences is possible by comparative examination of the nonhuman primates. Apart from male-initiated hetero- three indicators of female sexuality proposed by Beach sexual encounters it is possible that the degree of sexual (1976)—receptivity (readiness to copulate when copula- attractiveness of a woman might also be measured by tion is initiated by a male), proceptivity (active encour- the length of in relation to the phase agement of a male to copulate), and attractiveness of the cycle, the increase in attractiveness being re- (stimulus releasing sexual excitation in the male)—and flected in an increase in male sexual excitation and a one indicator for males proposed in this paper that reduction in the time required for ejaculation. Among Beach does not consider. rhesus monkeys, this latter time was found to be on the Research on the sexual behaviour of primates has average 5.4 minutes in the proliferative phase and 12.5 shown that in at least a few species of the Cercopithec- minutes in the (Wallen 1982), though, ad- oidea and the Hominoidea females very rarely refuse mittedly, under conditions of limited space the differ- copulation, and if they do it has to do with the particu- ences proved negligible (4.8 versus 6.3 minutes). lar male rather than with their hormonal state (having An indicator not considered by Beach but one of enor- refused one, they immediately copulate with another) mous importance for the analysis of sexual behaviour is (Chalmers 1979, Keverne 1987). Female orang-utans the sexual excitability of the male. Dependent on the (Pongo pygmaeus) (Maple 1980, Galdikas 1981), chim- endogenic level of androgen, this indicator may explain panzees (Pan troglodytes) (Lemmon and Allen 1978), the indiscriminate, intense sexual activity of young and (P. paniscus) (Badrian and Badrian 1984) males or males with high testosterone levels. The high- copulate irrespective of the phase of the cycle. These est frequency of copulation among baboons (Saayman data indicate that the loss of oestrus is a trend in some 1970), macaques (Zhao 1993), and (Tutin Haplorhinii and not a change that occurred only in the 1979) was observed in young males, and, while the fre- . Thus, constant receptivity as defined by quency of copulation increases in the ovulatory phase Beach (1976) is not a distinctive feature of H. sapiens, of the cycle in mature males, no such relationship ex- and hypotheses based on its species-specific character ists in juvenile (juvenis and subadultus) male baboons in the evolution of the Homininae are questionable. (Saayman 1970) or chimpanzees (Hasegawa and Hira- However, under another, less precise definition of re- iwa-Hasegawa 1989, Wallis 1995). Thus females are ceptivity, constant receptivity is understood as con- constantly receptive and males alone are selective as to stancy of the female’s sexual activity across her cycle. the choice of the period of copulation relative to their If receptivity is interpreted in this way, the parameters age and androgen level. An increase in this indicator differentiating the Homininae from the rest of the pri- may prevent the detection of changes in female procep- mates should be constant proceptivity and attrac- tivity and attractiveness. If this indicator in humans dif- tiveness. fers from that in other Hominoidea and some Cercopi- Although females of some nonhuman primate species thecoidea in that it remains high longer in relation to are constantly receptive, there is a distinct fluctuation the length of the reproductive period and may inhibit in the frequency of sexual behaviour relative to the the indicators of sexuality in women, it may be con- phase of the female cycle that results in part from nected with an extended period of development. De- changes in proceptivity and attractiveness. Nonhuman layed sexual maturity and longer duration of juvenile primate females express increased interest in males sexual behaviour in men are also suggested by the when levels of estrogen and testosterone are high, that longer period of immaturity of the hormonal system is, in the proliferative and ovulatory phases. This inter- regulating menstrual cycles and behavioural responses est is manifested by approaching males, presenting the in young women—expressed in less frequent ovulation, anogenital area, and encouraging them to copulate lesser capacity for progesterone secretion of the corpus (Wallis and Englander-Golden 1992). In most primate luteum and its lower level in saliva (Ellison et al. 1987, species the most frequent initiation of copulation by fe- cited by Ellison 1991), and lower frequency of secretion pawŁowski Loss of Oestrus and Concealed Ovulation 259 table 1 Proceptivity, Attractiveness, and Intercourse Frequency by Phase of the Menstrual Cycle in Homo sapiens

Phase of Menstrual Cycle

Menstrual Proliferative Ovulatory Luteal Premenstrual No Change

Proceptivity Autosexual behaviour ϩ (3) ϩ (1, 2) ϩ (3) Female-initiated sexual ϩ (1, 3) ϩ (1, 2, 4) (5, 6) encounters Sexual thoughts and ϩ (9) ϩ (4, 7, 8, 9) ϩ (7, 16) ϩ (7, 9, 16) (5) fantasies Sexual desire ϩ (7, 10, 11, 12, 13) ϩ (7, 11, 13) ϩ (12) ϩ (10) Number of orgasms ϩ (4, 14) Othera ϩ (15) Attractivenessb ϩ (1, 2, 16) Intercourse frequency ϩ (2 plus 10 of 12 ϩ (6 of 12 stud- Ϫ (12 studies ϩ (4 of 12 studies col- ies collated collated studies lated by Hill by Hill 1988) by Hill collated 1988) 1988) by Hill 1988) note: ϩ, increase in comparison with other (or, in the case of bimodal data, previous) phases; Ϫ, decrease in comparison with previ- ous phase. sources: 1, Adams et al. (1978, cited by Hill 1988); 2, Harvey (1987); 3, Bancroft et al. (1983); 4, Matteo and Rissman (1984); 5, Spitz et al. (1975, cited by Hill 1988); 6, Persky et al. (1978, cited by Hill 1988); 7, Markowitz and Brender (1977, cited by Hill 1988); 8, Sanders et al. (1983, cited by Hill 1988); 9, Zillmann, Schweitzer, and Mundorf (1994); 10, Tinklepaugh (1933b, cited by Hill 1988); 11, McCance et al. (1937, cited by Hill 1988); 12, McCullough (1973, cited by Hill 1988); 13, Dennerstein et al. (1994); 14, Udry and Morris (1968); 15, Daly and Wilson (1983:318); 16, Englander-Golden et al. (1980, cited by Hill 1988). aE.g., increase in intensity of makeup. bAs measured by male-initiated encounters. of this hormone in the luteal phase in women under 22 ality in both females and males show fluctuations de- years of age than in women of similar height and weight pendent on hormone levels, an approximately similar between 23 and 35 (Thorne 1988, cited by Ellison 1991). distribution of sexual activity in females should be ex- This phenomenon may create a slight negative proges- pected here. terone effect that influences proceptivity and attrac- Field data on all the nonhuman primates indicate the tiveness in young women. Thus neoteny and the highest frequency of sexual activity in the ovulatory lengthening of the period of endocrine-system immatu- phase of the cycle. For many it increases in the prolifer- rity in H. sapiens may disrupt the behavioural manifes- ative phase and immediately before . This tations of the physiology of this system with regard to is consistent with the fluctuations of hormonal secre- sexuality. This is significant for research on the sexual tions and confirms the results of research on proceptiv- activity of women, where consideration of the ages of ity and attractiveness. In chimpanzees (Wallis 1982, their partners (and, even better, the latter’s androgen 1992), macaques (Herbert 1974, cited by Wallis and En- levels) would permit the identification of the male ex- glander-Golden 1992), and baboons (Saayman 1972), citability factor that may mask the indicators of female most copulation occurs at the time of anogenital swell- sexuality. If the group of women under study has young ing, that is, during the proliferative and, in particular, male partners with very high levels of testosterone, the ovulatory phase of the cycle. In primates in which fluctuation of the frequency of sexual activity in rela- there is no such swelling, the distribution of copulation tion to the phases of the cycle may be impossible to re- is similar, that is, most sexual activity occurs in the cord (as has been found in chimpanzees [Hasegawa and ovulatory phase of the cycle. This is by no means to say Hiraiwa-Hasegawa 1989, Wallis 1995]). This may be the that copulation is absent in the other phases of the cy- reason that fluctuations in sexual activity are not re- cle. Very convincing data in this respect are available corded in female college students (although other rea- for the gelada, in which Dunbar (1978) found a more sons could be more frequent refraining from sexual con- even distribution of copulation during most of the cy- tact at the time of increased probability of becoming cle, and for the crab-eating macaque (Macaca fascicu- pregnant or more frequent changing of partners). Young laris) (Noordwijk 1985), in which no relationship be- chimpanzees also copulate twice as often as mature ani- tween the frequency of copulation and the degree of mals (Hasegawa and Hiraiwa-Hasegawa 1989). Since in swelling was found. The stump-tailed macaque (M. arc- at least a few species of primates the indicators of sexu- toides), which does not display outward signs of ovula- 260 current anthropology Volume 40, Number 3, June 1999 tion, also copulated throughout the cycle (Nieuwehuij- 1990), indicating an increase in the sexual indicators sen 1985, cited by Hrdy and Whitten 1987). This and in sexual excitability in this period. behaviour intensifies only slightly in the ovulatory The changes recorded in the indicators of sexuality phase of the cycle in the vervet monkey (Cercopithecus and the uneven distribution of sexual activity across the aethiops) (Andelman 1987) and the Geoffroy’s tamarin menstrual cycle indicate that sexual behaviour cannot (Saguinus oedipus) (Brand and Martin 1983). Copulation be considered independent of the physiological period- independent of ovulation or hormone levels has also icity of functional changes in the endocrine-system been observed in the Japanese macaque (M. fuscata) glands associated with human reproduction. If the pro- (Nigi, Hayama, and Torii 1990). These data confirm that liferative and ovulatory phases were considered to- the absence of oestrus is quite frequent in the primate gether, the consistency in the distribution of sexual ac- order; it seems to be the evolutionary trend in this tivity between, for example, chimpanzees or macaques group of animals (see Dunbar 1988, Martin 1992) and and humans would be even greater. That selection has not a unique phylogenetic acquisition of the Homi- favored the intensification of sexual contacts before ninae. ovulation is biologically reasonable. The variability of Hill (1988) collected data on 12 groups from ten re- gestation in the Anthropoidea (4%) is greater than in search projects on the frequency of copulation in rela- other mammals (including the Prosimii) (2.1%), and it tion to the menstrual cycle and found that the number may be suggested that either the spermatozoa of this of sexual contacts decreased during ovulation (in rela- group of animals are more vital (lasting longer than 48 tion to the preceding phase) in only three. Given that hours) or ovulation is longer (although more frequent two of these three studies involved female college stu- occurrence of multiple ovulations in a cycle and in- dents, the decrease in the number of sexual contacts duced ovulations are other possibilities) (Martin 1992). may be attributed to the desire to avoid intercourse in These data indicate that hypotheses regarding the be- this period because of the fear of pregnancy. Where havioural evolution of humans that emphasize the there is no or fear of pregnancy, uniqueness of the absence of oestrus are debatable, fluctuation of sexual activity in relation to the phases of however marked the phenomenon. the menstrual cycle is clearly observable. The greatest number of instances of sexual self-excitement in women (1.6 times more frequent than in the menstrual phase) was observed in the ovulatory phase of the cycle Ecological and Cultural Influences on the (Harvey 1987). A considerable increase in sexual con- Distribution of Sexual Activity tacts in the ovulatory phase and their decrease in the luteal phase was also recorded in lesbian women When women subjects are unaware of the aim of the re- (Matteo and Rissman 1984). search on their sexual activity, they manifest a consid- The data presented by Hill (1988) also show that no erable increase in sexual excitability in the middle, pre- decrease in the frequency of sexual contacts in the pro- menstrual, and postmenstrual phases of the cycle, and liferative phase was recorded in any case and in ten otherwise their responses are the reverse (Englander- cases a considerable increase was observed. It was in Golden et al. 1980, cited by Wallis and Englander- fact in the luteal phase that there was no increase in the Golden 1992). Moreover, results corresponding to the frequency of sexual activity in any of the groups. In four expected bimodal distribution of sexual activity tend to cases the increase was recorded before menstruation, be achieved when the data are collected soon after the and these data correspond to the similar increase in the events and not with retrospective data (Manson 1986). same phase of the cycle in macaques (Keverne 1976, Even if objectively recorded, however, the indepen- cited by Chalmers 1979). This phenomenon is linked dence of sexual activity from hormonal factors that is with the considerable decrease, just before menstrua- so often emphasized in research on the evolution of hu- tion, in the level of progesterone. This increase in sex- man sexual behaviour may have a variety of causes. ual activity both in the ovulatory phase of the cycle and Rather than requiring, as the majority of researchers before menstruation is so characteristic of some pri- propose, the pressure of sexual selection, it may be ex- mates (including humans) that Manson (1986) has pro- plained as the result of the influence of ecological and posed a bimodal curve for its distribution. cultural factors. Harvey (1987) observed that women, similarly to Sexual behaviour is influenced by such living condi- men, show maximum initiative in heterosexual activ- tions as the space occupied and, in the case of social spe- ity precisely during ovulation. She found a correspon- cies, the isolation of the heterosexual couple. The area dence between the fluctuation of this behaviour and the of the available space occupied by male and female rhe- fluctuation of estrogen levels across the cycle (increas- sus monkeys (M. mulatta) significantly influences sex- ing from menstruation until the ovulatory phase and ual activity (Wallen 1982), and spatial parameters of the then decreasing through the luteal phase until menstru- environment influence the frequency and distribution ation). It is interesting that the number of sexual con- of sexual activity in all apes (Graham and Nadler 1990). tacts with other than regular partners is greatest in the In limited space (a cage) the frequency of copulation has ovulatory phase of the menstrual cycle (Bellis and Baker proved to be independent of the phases of the female’s pawŁowski Loss of Oestrus and Concealed Ovulation 261 cycle. Male gorillas, orang-utans, and chimpanzees ovulatory phases and there is a link between increased caged with a female display increased frequency of sex- level of steroids in the blood, frequency of sexual activ- ual activity (e.g., chimpanzees [Butler 1974] and orang- ity, and number of orgasms. The level of testosterone utans [Heinrichs et al. 1970, cited by Butler 1974] copu- in Ache men is lower than in men of Western societies late every day), but when the female decides on the (Bribiescas 1994), and, more interesting, Ache who have male’s access the frequency is comparable to that re- recently shifted to agriculture display higher testoster- corded under natural conditions (Graham and Nadler one levels than those who remain hunter-gatherers. 1990). Thus, the reactions of males under such condi- Thus the change of economy in the Neolithic may, tions are more strongly affected. The presence of other through a change in hormone levels, have influenced males (especially outsiders) stimulates greater sexual some indicators of sexuality (e.g., male excitability) and activity independent of the phase of cycle in both males thus caused the flattening of the distribution of sexual (e.g., in the macaque and the gorilla) and females (e.g., activity across the menstrual cycle. in the langur and the gelada) (Zhao 1993). Under such The considerable influence of cultural factors on sex- conditions, accompanied by the weakening of other se- ual behaviour is indicated by the fact that fluctuation lective pressures, hypersexuality becomes adaptive. In of sexual activity with the phases of the menstrual cy- the absence of selective factors distinguishing individu- cle has been recorded in African-American female man- als in terms of fitness in acquiring food, avoiding preda- ual workers and not in educated European-American tors, or adapting to climatic changes, increase in sexual housewives (Udry and Morris 1968). Education of activity and consequently fertility become decisive for women and men has proved decisive in avoidance of individual fitness. No periodic changes in proceptivity sexual intercourse in the menstrual phase (Barnhart, and attractiveness were recorded in the stump-tailed Furman, and DeVoto 1995); a university degree is linked macaque (Slob et al. 1978, cited by Hill 1988) and the with less avoidance of sexual contacts in this phase and pig-tailed macaque (M. nemestrina) (Easto and Resko thus with a more even distribution of this behaviour 1974, cited by Hill 1988) under laboratory test condi- across the cycle. tions when the couple was isolated. Great differences in Another factor affecting the distribution of sexual ac- the frequency of sexual activity in the and the tivity across the menstrual cycle may be the culturally chimpanzee to the advantage of the bonobo may result imposed weekly and daily rhythms associated with par- from the time the two sexes spend together (nearly ticular types of work. On working days, from Monday 100% in the bonobo and less than 40% in the chimpan- to Friday, the frequencies of copulation are similar and zee) (after Wrangham 1993). Proceptivity and attrac- relatively low, whereas they increase considerably on tiveness are indicators of considerable importance un- Saturdays and almost double on Sundays (38.3% of cop- der natural conditions, as their function is to reduce the ulations take place on weekends) (Palmer, Udry, and physical distance between male and female, that is, to Morris 1982). This evolutionarily quite new seven-day form couples (Hill 1988). Under conditions that require periodicity may influence the distribution of sexual ac- animals to spend most of their time together in limited tivity across the menstrual cycle, perhaps postponing space, the variability of these two factors loses its sig- its peak for a few days. A similar dependence of the in- nificance. tensity of sexual activity on the distribution of work The decline in importance of many selective factors time and time off was also found by Silber (1994). that once differentiated individuals in terms of fitness Because research on the sexual behaviour of modern and the increase in group density and domestication humans reveals its dependence on the phases of the may have played a considerable role in the evolution of menstrual cycle, this phenomenon must have been human sexual behaviour. Confinement to a hut or shel- present in all the earlier stages of the evolution of the ter of some kind and the constant physical presence of Homininae. It is very probable that because of the ab- an individual of the opposite sex may have flattened the sence of hygiene inhibiting olfactory communication, curve of the distribution of sexual activity across the cy- the absence of clothing under African climatic condi- cle in H. sapiens as in the other primates (e.g., talapoins, tions, the relatively high daily air temperatures, which macaques, baboons, gorillas, orang-utans, chimpanzees facilitated evaporation and the reception of pheromonal [Keverne 1987]) living under similar conditions. signals, the necessity of greater involvement in the pro- Hormonal physiological parameters in the women of tection and acquisition of food at the expense of sexual hunter-gatherer and horticultural societies are different activity, and the absence of many of the cultural factors from those of Western women. A relatively low level of influencing sexual behaviour, the periodicity of this be- hormone production by the female gonads (Rosetta haviour was greater than the research on modern hu- 1995) has been recorded in non-Western societies. Be- mans indicates and approximated that of other pri- cause of the hormonal conditioning of sexual behav- mates. The sexuality of H. sapiens calls into question iour, both the importance of this behaviour and its dis- both the view that a new type of such behaviour tribution across the menstrual cycle may be different in emerged as early as in the Plio/Pleistocene evolution of these societies. Research on !Kung San women (Worth- the Homininae and the attribution of substantial homi- man 1978, cited by Hrdy 1981) revealed that the fre- nizing functions to this phenomenon. If differences are quency of copulation increases in the proliferative and observed, they tend to be quantitative rather than quali- 262 current anthropology Volume 40, Number 3, June 1999 tative in character, and they may be explained as side Homininae. This is the reason that hypotheses con- effects of certain ecological-cultural factors rather than cerned with the disappearance of this feature in anthro- in terms of the direct operation of sexual selection in pogenesis are advanced. the early stages of anthropogenesis. The development of Although concealed ovulation is to be understood as tool making and use connected with encephalization the absence of external signs of ovulation—visual ones and the use of fire and the construction of shelters also such as swelling of the anogenital area and olfactory and meant substantial liberation from the selective pressure behavioural signals—many writers, as Sille´n-Tullberg of predation and climatic and alimentary factors. Only and Møller (1993) point out, consider ovulation as con- then could the fitness benefits of fertility associated cealed in the absence of its visual signs only. Because with sexuality assume major importance. The excess of this phenomenon occurs very often in the primates free time itself, accompanied by the implementation of (Dixson 1983, Andelman 1987, Sille´n-Tullberg and effective technologies for food acquisition and the Møller 1993), interpreting it as specifically human and lengthening of the day because of the control of fire may connected with hominization seems unjustified. Ovula- have been very important elements in certain changes tion is also concealed in the case of anogenital swelling in sexual behaviour. Even in historical times the differ- in the bonobo, which lasts for 48% of the cycle al- ences between societies (e.g., 6.8 sexual contacts per though the ovulatory phase lasts only two to three days month for women between 20 and 24 in Bangladesh ver- (after Wrangham 1993). It is not the absence of signs of sus 9.5 for women under 25 in the U.S.A. [Udry, Deven, the brief moment of ovulation that is the issue here but and Coleman 1982]) and between social groups (e.g., the possible evolutionary change in this signaling. The the aristocracy and the lower social strata) indicate proponents of the view based on the chimpanzee model that economic conditions and the amount of free time maintain that evolution inhibited or reorganized the are very important in differentiating sexual behaviour once-distinct signals of the fertile phase of the cycle in as well. It is hardly surprising, then, that the distribu- the line of the Homininae. The question is whether tion of sexual activity across the menstrual cycle may such a change in fact took place in the evolution of the have been flattened more in some societies than in Homininae and, if so, whether its causes were con- others. nected with sexual selection and its effects were sig- The evolution of the Homininae was accompanied by nificant for social structure. considerable climatic change, which altered the physi- Adopting the chimpanzee model for many morpho- cal environment in terms of both the daily and the an- logical and behavioural features does not mean that sex- nual cycle. The changing environment may have called ual swelling similar in intensity to that in the chimpan- for a more flexible behavioural response, and this may zee was present in prehominines. Dixson (1983) have led to greater independence of the functions of the concludes that prehominines did not have this feature endocrine system from the environment and somewhat at all. In the Hominoidea swelling and reddening of the relaxed the strict hormonal control of human behav- skin in the anogenital area in the proliferative and ovu- iour. latory phases of the cycle occur only in the chimpanzee. His proposal is accepted by Hrdy and Whitten (1987), who maintain that, given that the pink swelling is ab- sent in the majority of primate species, this feature is Signs of Ovulation in the Evolution of the the basic and original condition in the primates and the Homininae appearance of the in the Hominoidea is specific to Pan. It seems that although many changes The very fact of intensification of sexual activity in the are emphasized in modeling the evolution of humans, proliferative and ovulatory phase of the menstrual cycle changes in the model species are too often neglected. confirms the view that ovulation in humans is not com- Undoubtedly many changes have occurred in the genus pletely concealed. The variation of proceptivity across Pan since it diverged from the line leading to Homo, the cycle indicates the existence of behavioural signal- that is, in the course of the past 5–7 million years. ing of the fertile phase of the cycle. This behaviour is Chromosome analysis (Yunis and Prakash 1982) indi- influenced by endogenic factors whose action was evo- cates the occurrence of a greater number of chromo- lutionarily fixed as one of the mechanisms increasing some changes in the evolution of the chimpanzee than the chance of conception. Because the signaling is not in humans. Considering the absence of visible remnants controlled by rational thought and need not be per- of this feature in Homo and assuming evolutionary spe- ceived as such, it may seem absent. In addition to be- cialization in the direction of multimale social struc- havioural signaling, there may be visual and olfactory ture in the chimpanzee after the divergence of the lines signaling as well. leading to Pan and Homo, it seems probable that this Visual signals of ovulation involving swelling of the feature was absent in the prehominines. anogenital areas are absent in modern humans. There Yet the occurrence of at least slight anogenital swell- would not be anything unusual about this—most pri- ing in the evolution of the Hominoidea is indicated by mates, including most hominoids, lack such manifesta- its original presence in the Cercopithecoidea (Sille´n- tions—if it were not for their occurrence in the chim- Tullberg and Møller 1993) and its vestiges in the puden- panzee, the model animal for the evolution of the dal-lip swelling in the ovulatory phase of the cycle in pawŁowski Loss of Oestrus and Concealed Ovulation 263 the gorilla (Nadler 1981) and the swelling during preg- of the evolution of the Homininae could, however, have nancy in the orang-utan (Galdikas 1981) in the same influenced this feature. way as in the chimpanzee (Wallis and Goodall 1993). Probably the simplest explanation is as a side effect If this feature occurred in the prehominines and its of . Erect posture changed the position of the basic development is to be connected with the evolu- female external genitals and concealed them between tion of the line of Pan, slight anogenital swelling in the the legs, and thus swelling as a mode of signaling be- proliferative and ovulatory phases of the cycle would be came useless (Tanner 1981). Selection may have favored a more appropriate model for this line. That the swell- females who did not have the periodic problems with ing was slight in the phylogeny of humans is substanti- bipedal locomotion caused by considerable anogenital ated by the cladistic analysis of this feature in the pri- swelling (Gallup 1982). However, the evolution of bipe- mates conducted by Sille´n-Tullberg and Møller (1993), dalism was a long-term process. Despite some disagree- who postulate that the original state in the prehomi- ment (see Kozieł 1994), it seems that the mode of loco- nines and all of the Hominoidea was only slight swell- motion of the first Australopithecus differed from that ing and reddening of the anogenital area. Similarly to of the later forms and may have been intermediate be- Dixson (1983), they tend to accept the idea that the ex- tween those of contemporary apes and of humans treme swelling of the anogenital area is specific to the (McHenry 1991, among others). If swelling was less in chimpanzee. the prehominines than in the chimpanzee, it would not The idea that there may have been some such swell- have had so much influence on female locomotion. ing in the prehominines and the early Homininae is In addition to bipedalism, which changed the position supported by the considerable length of the penis in of the genitals, the change of the line of vision (males Homo. The lengthening of this organ took place in the could no longer constantly see the female genitals) primates that have anogenital swelling—the chimpan- could have been another reason for the loss of function- zee, the stump-tailed macaque, the , and the ality of this feature. The change of environment for a yellow baboon (P. cynocephalus). In nonhuman homi- more open one in which the Homininae were subject to noids lacking anogenital swelling—the gorilla, the or- greater danger from predators may have increased the ang-utan, and the gibbon—the penis is almost invisible. density of the population, and in such a case this feature Swelling increases the depth of the vagina (at maximum may have lost its function of long-distance sexual sig- swelling in the chimpanzee it increases as much as 52% naling. At the same time, selective pressure toward an [Dixson and Mundy 1994]), and proper penetration re- increase in the amount of adipose tissue and its reserves quires the longer penis. Dixson and Mundy report that in the buttocks area caused the replacement of the sex- in 11 chimpanzee males the length of the penis at erec- ual swelling, sensitive to the action of estrogen, by adi- tion was 11–19 cm, with an average of 14.4 cm, thus pose tissue. The loss of functionality need not have only slightly less than in H. sapiens. Yet, because of the caused the disappearance of this feature if the cost of evolution of bipedalism and the abdominal relocation maintaining it was negligible, but swelling increases of the female external genitals, the lengthening of the the weight of a female (in P. ursinus by 8–10% [Bielert human penis does not need to be explained in terms of and Busse 1983, cited by Zinner, Schwibbe, and Kau- so great a swelling of the female as in the chimpanzee. manns 1994] and in M. nemestrina by 17% [Dixson Bipedalism itself seems an insufficient explanation for 1983]) and adds to the energetic cost of locomotion for the 15–17-cm length of the erect penis (Imielinski at least several days. Other possible additional costs of 1985). With an average vagina depth of ca. 10–12 cm anogenital swelling could have been specific to the line (Imielinski 1985), approximating that of the chimpan- of the Homininae. In the new savannah environment zee (ca. 12.5 cm [Gould and Martin 1981]) or 12.6 ϩ 1.69 the thermoregulatory system may have been modified cm [Dixson and Mundy 1994]), such a long penis is not in order to conserve water. Under such conditions indispensable. Therefore it is possible that its ‘‘extra’’ swelling involves an additional cost (ca. 1.5 liter in the length is connected with the existence of slight swell- chimpanzee), and effective evaporation of sweat on the ing in an already bipedal female. The situation of the swollen area is hindered by its location in the area of relaxation of the penis-elongation selection factor— humid vegetation in the savannah environment. Fur- that is, the retreat of swelling and a long penis—occurs thermore, because of the loss of hair and the risk of hy- in the stump-tailed macaque. What remains to be ex- pothermia at night (Pawłowski 1998) the loss of heat plained is the disappearance of relatively slight visual through the highly hyperaemic sexual swelling would signs of ovulation in the Homininae, a vestige of which, have been a disadvantage. in the form of periodic (estrogen-dependent) peripelvic If the slight swelling was present in the early Homini- hyperaemia, occurs in H. sapiens as well (Wallis and En- nae, there may have been many physiological and mor- glander-Golden 1992). phological reasons other than sexual or social ones for Irrespective of the model accepted for the prehomi- its disappearance. The reduction of the anogenital nines (chimpanzee or gorilla, the latter proposed by swelling in the gelada (Theropithecus gelada) is consid- Schro¨ der [1993 a, b]) and on the assumption of the exis- ered to have been caused by its atypical way of feeding tence of anogenital swelling, the disappearance of this (most of the time in a sitting position) (Dixson 1983). feature is usually explained in terms of sexual selection The reduction of the sexual swelling in some species of for a change in reproductive strategy. Certain features macaques (Dixson 1983) cannot be linked to changes in 264 current anthropology Volume 40, Number 3, June 1999 social and reproductive structure, for these were not al- connected with the fact that it is situated close to the tered. organ perceiving the signals (the nose). Compared with Thus, seeking evolutionary explanations for the dis- the anogenital area, the axillary organ is situated closer appearance of this exaggerated feature in sexual selec- to the level of the receptor of olfactory signals in the tion and behavioural selection pressure that resulted in bipedal Homo than in the gorilla and the chimpanzee, the emergence of new social structures seems inappro- and for this reason it is best-developed in this species priate. There were many more fundamental adaptive (Stoddart 1990). Because the armpit is almost closed, in- changes, and they included changes (often as side ef- tensive sweating is irrelevant for thermoregulation, and fects) in the features just discussed. the changes in the size of the axillary glands and the smell of the sweat of a woman in relation to the phases of the menstrual cycle (that is, to hormone levels) con- firm their signaling, pheromonal functions (Mykyto- Olfactory Sexual Signaling in Human wicz 1985). The high development of the axillary organ Evolution in the majority of modern humans may be a form of compensation for the reduced role of vaginal phero- Although the evolutionary trend in the primates is the mones. According to Tanner (1981), the concealed geni- development of tactile-visual perception and selection tals and enlarged buttocks caused by bipedal locomo- oriented toward the development of parts of the brain tion prevented the spread of , and the unconnected with smell, olfactory communication per- considerable distance between the vagina and the nos- sisted. Because of the limbic projection of the olfactory trils of upright males resulted in a lower concentration system and its closer connection than in the case of of pheromones reaching the olfactory organs. This may hearing and sight with the centers of emotion, signals have reduced the role of female pheromones in intersex- perceived in this way are often subconscious (Stoddart ual communication. Yet, the signaling persists, as the 1990, Schleidt 1992). This may be the reason that this increase of estrogens in the proliferative phase of the cy- type of communication is underestimated. Recent re- cle is accompanied by an increase in copulines (volatile search shows that H. sapiens cannot properly be de- fatty acids) whose production depends on the vaginal scribed as a microsomatic creature (Schaal and Porter bacterial flora. The odor of vaginal secretions is per- 1991). The actual sizes of the bulb in apes and humans ceived as pleasing only in the ovulatory phase of the cy- are similar. Although the mucosa of the human nose cle (Stoddart 1990). have fewer receptor cells than those in the other mam- That both pubic and axillary hair develop during pu- mals, the quantity of olfactory substances produced by berty is a reflection of their function in olfactory com- humans is almost the largest of all the primates (Stod- munication. Hair provides an additional area for the ac- dart 1990). Did chemical signals perceived with the tivity of the microorganisms involved in producing the sense of smell and the odorless, nonvolatile ones per- odor, and being springier than head hair it enhances the ceived by the rudimentary vomeronasal organ (Stensaas diffusion of the secretions. Its importance in dissemi- et al. 1991, Cohn 1994) have any influence on the physi- nating chemical signals is indicated by the fact that ology of reproduction and reproductive behaviour in the after thorough washing of the armpit with soap the typi- evolution of the Homininae? cal odor reappears within 6 hours in an unshaven arm- From the point of view of the number, size, and pro- pit but only after 24–48 hours in a shaven one (Shelley duction of the sebaceous and apocrine glands, humans et al. 1953, cited by Schaal and Porter 1991). are the smelliest hominoids. Characteristically, the se- The perception of these chemical signals by the olfac- baceous glands are three times more active during pu- tory mucosa and the vomeronasal organ may be con- berty, when the apocrine and apoecrine glands develop, scious and/or unconscious and may take a variety of and their occurrence mainly in places such as the arm- forms. In the rhesus, swelling and reddening of the mu- pits, the areola mammae, and the navel, pubic, and ano- cosa of the nose are as much dependent on hormones as genital areas indicates that their function is connected anogenital swelling. The mucosa of the nose are stimu- with reproduction (Stoddart 1990). lated by hormones, and the sympathetic nervous sys- Homo, Pan, and Gorilla contrast with the other pri- tem is connected with changes in their sensitivity to mates in having axillary organs (Cohn 1994), their loca- odors. When the amount of estrogen increases during tion in the armpit being marked by perpendicular rows ovulation and pregnancy, swelling and reddening of the of hair with the accompanying sebaceous, apocrine, and mucosa of the nose also occurs in women (Mykytowicz eccrine glands. Here the odor involved in olfactory com- 1985). munication is produced and diffused with the coopera- Although the data on olfactory communication in tion of microorganisms. It is dissolved in the watery se- connection with reproductive behaviour in humans are cretion of the eccrine glands, and it is similar for all inconsistent, enough is known to demonstrate its in- three taxa (Montagna 1985). Spielman et al. (1995) fluence on the menstrual cycle, sexual activity, and maintain that chemical signaling by the axillary organ even mate selection. Among the evidence for this are performs the same pheromonal function as in the other the following findings: mammals. The secretion of pheromones by this area in 1. The synchronization of the menstrual cycles of an animal of partly or fully erect posture is probably women living together (McClintock 1971, Graham and pawŁowski Loss of Oestrus and Concealed Ovulation 265

McGrew 1980) and the fact that this synchronization posture, which moved the receptor of these signals has been found to occur in women whose upper lips away from the anogenital area that was their main were rubbed with diluted axillary secretion of another source. It was perhaps at this point, however, that the woman (Russell, Switz, and Thompson 1980, Preti et al. axillary organ shared with Pan and Gorilla became en- 1986, Stern and McClintock 1998). larged, and the fact of this enlargement is evidence of 2. The influence of the presence of a man on the selection directed toward maintaining this signaling. length of the menstrual cycle, with occasional sexual Under the conditions of the open savannah, with contacts and celibacy being associated with increased abundant sunshine, and the increased secretion of the frequency of irregular (Burleson, Gregory, and Treva- olfactory glands caused by work, olfactory signaling was than 1991) or nonovulatory cycles and greater regularity sufficiently intensive to perform its function. Increased and shorter cycles with the influence of the male axil- body temperature allowed greater development of sym- lary secretion only (Cutler et al. 1986, cited by Stoddart biotic microorganisms and increased enzymatic activ- 1990). ity, increased secretion of the sebaceous glands (by 10% 3. An increase in sexual activity under the influence with an increase in skin temperature of 1°C), and more of the axillary odor of a woman (Cutler 1987); here the rapid volatilization of olfactory substances and greater involved seems to be , which effectiveness of olfactory stimulation (Schaal and Porter has been found most abundant in the axillary secretions 1991). As the temperature of breathed air increases, the of women in the middle of the proliferative phase of the mucosa of the nose are altered, with qualitative changes cycle (Stoddart 1990). in the perception of odors (Schaal and Porter 1991). 4. The influence of androstenol and androstenone on With the increase in secretion of the axillary organ un- the assessment of the attractiveness of individuals der hot savannah conditions, olfactory signaling could (McCullough, Owen, and Pollack 1981, Filsinger, perform its communicative functions in the sexual con- Braun, and Monte 1985). text without any substantial change. More important, 5. The lowering of the threshold of sensitivity at the with selection directed toward increase in the signifi- end of the proliferative phase and in the ovulatory phase cance of other forms of communication, these condi- of the cycle (Doty et al. 1981, cited by Stoddart 1990), tions did not require any proportional increase in olfac- when even androstenone is perceived more positively tory signaling. than in other phases (Grammer 1993). Reduction of the One factor that may have prevented more olfactory negative reception of this odor facilitates sexual ac- signaling in early forms of Homo is the greater density tivity. of the group connected with protection against preda- 6. The perception of pheromonal signals by men un- tors and the need to stay close together during colder der laboratory conditions (Reynolds 1991). The odor as- nights. Under conditions of increased radiation in open sociated with the vaginal secretion may be perceived space under a cloudless sky, the temperature on the consciously, and it has the greatest concentration of ground may have dropped at night to the point that the volatile free fatty acids and the most pleasing smell in Homininae, who had little if any hair (Wheeler 1984), the ovulatory phase of the cycle (Keith et al. 1975, cited had to avoid excessive heat loss. One solution might by Wallis 1985). have been gathering in groups as is done, for example, 7. The possibility that mate selection is linked with by contemporary Pygmies (Turnbull 1986). In such situ- MHC (major histocompatibility complex)-dependent ations olfactory communication may have become too body-odor preferences associated with the immunologi- intense and selection may even have favored its reduc- cal recognition of peptides (Wedekind et al. 1995). tion. Androstenone, perceived negatively by both sexes Women who do not use hormonal contraception per- and linked with male rivalry and territoriality, may ceive the odor of a man as more pleasing when his MHC have prevented too close contact of individuals not just differs more from their own. at night. A decline in the production of this pheromone Most of this research shows that olfactory communi- may have attenuated antisocial, aggressive behaviour cation in connection with reproductive behaviour is of- within the group. Yet the reduction of the role of the ten subconscious. Thus periodic changes in the degree sense of smell with the parallel development of other of attractiveness are rarely connected with periodic forms of communication did not result in the loss of sig- changes in this form of signaling. Greater importance is nificance of this signaling. There seems to have been no attributed to the so-called vomeroferrines, the chemical selection directed against this mode of communication, substances perceived by the vomeronasal organ, which especially since it was already weakened in Australo- influence electrical changes and the temperature of the pithecus. Despite the absence of visual preovulatory skin. What is more, Montibloch et al. (1994) have dem- and ovulatory signs, olfactory communication was, to- onstrated sexual dimorphism in the mode of reception gether with behavioural signals, sufficiently strong to of these signals. cause intensification of sexual activity in the fertile pe- If olfactory signaling influences reproductive behav- riod of the cycle, as is the case in the gorilla and the iour in the contemporary civilized societies of H. sapi- orang-utan. ens, it must have been even more significant in the ear- The reason olfactory signaling has such limited sig- lier stages of human evolution. The original reduction nificance in human reproductive behaviour, especially of olfactory signals may have been a side effect of erect where clothing is worn, may be weaker olfactory condi- 266 current anthropology Volume 40, Number 3, June 1999 tioning in infancy. Olfactory experiences are well re- characteristic of the line leading to H. sapiens but an membered and associated with the limbic structures of evolutionary trend in the Hominoidea. the brain, and good olfactory memory (Schleidt 1992), especially of odors perceived in childhood, must be sig- nificant for reproductive behaviour. Experiments on ro- Conclusions dents have shown that the olfactory environment in the very early stages of life has considerable influence on Hypotheses of an evolutionary basis for the absence of later behaviour associated with olfactory communica- signs of ovulation and for strong sexual selection due tion (Fillion and Blass 1986). If ‘‘imprinting’’ of odors to loss of oestrus in human evolution are controversial. that influence later behaviour similarly occurs in hu- Constant receptivity is not species-specific, occurring mans, the abandonment of breast feeding, hygiene (of- in at least several other species of primates. It should ten accompanied by deodorants and perfumes), separa- not be attributed such evolutionary significance in the tion of mothers from infants during sleep, and shaving line of the Homininae, and it should not be the justifi- of the axillary hair by nursing mothers may have con- cation for the specific character of human social struc- siderably altered the conditioning of reactions to odors. ture and reproductive strategy. As in the other primates, In hunter-gatherer societies and even more in the earlier there is fluctuation in sexual activity with changes in evolution of the Homininae, infants were in almost proceptivity and attractiveness in the female cycle. The constant contact with their mothers. They were subject flattening of the curve of the distribution of sexual ac- to olfactory conditioning all the time and not just dur- tivity seems to be a definite evolutionary trend in many ing feeding as in contemporary clothes-wearing socie- anthropoids. The differences in degree of the distribu- ties. Study of two-week-old infants revealed that if they tion of this activity between humans and the other pri- were breast-fed they differentiated between the axillary mates can to some extent be explained in terms of the odor of their mothers and those of other women (Cer- endocrinological, ecological, and cultural conditions. noch and Porter 1985). Research on olfactory sensitivity They need not be the product of specific selective pres- to pheromones should perhaps take into consideration sure favoring a new type of reproductive strategy. the type of feeding in infancy. It may be that the main Similarly, the disappearance of visible signs of ovula- function of the apocrine and sebaceous glands on the tion in the course of the evolution of the Homininae areola mammae, apart from protecting the skin against need not be associated, as in the other primates, with the caustic action of the saliva, is pheromone condition- selection directed toward a new type of reproductive be- ing of infants. The plexus venosus areolaris raises the haviour. Rather, it may be the consequence of the evo- temperature of this area in relation to the rest of the lution of bipedalism and of environmental conditions. breast, and this along with the higher temperature of If hunter-gatherer societies and even Western ones have the armpits may increase the rate of volatilization of semiochemical and behavioural signaling that affect pe- the olfactory substances and thus their semiotic effec- riodic changes in sexuality indicators and a bimodal dis- tiveness (Schaal and Porter 1991). tribution of sexual activity, this signaling must have In considering the earlier stages of human evolution been present to a greater extent in all the earlier forms it should be assumed that olfactory communication in of the Homininae. The absence of visual signaling of the context of sexual behaviour played a greater role ovulation could have allowed these forms greater flexi- than it does in contemporary H. sapiens. Absence of in- bility in the choice of a reproductive strategy adaptive tensive hygiene, the influence of pheromones secreted under particular ecological and cultural conditions. by the apocrine glands on the breast and by the axillary Such behavioural adaptation was the effect of other evo- organ, and, to a certain extent, pheromones from the va- lutionary changes in this line (e.g., bipedalism, brain- gina of the nursing mother could have conditioned the size increase, the change in the rate of individual devel- imprinting of the attractiveness of these odors and sen- opment) and not the direct cause of a change in social sitivity to them in the context of later sexual behaviour. structure and the effect of sexual selection. It must be borne in mind that, like the loss of oestrus, To attribute these very significant evolutionary the diminishing significance of olfactory communica- changes in the process of hominization to sexual selec- tion is an evolutionary trend in the primates. In the tion is questionable. The considerable flexibility of the chimpanzee neither the amount of copulines nor their species in terms of reproductive strategies demonstrates qualitative change in the course of the female cycle is both the influence of various ecological factors on re- a sufficient olfactory signal for males, for these do not production and the absence of evolutionary selective vary enough by phase of the cycle (Fox 1982). Although pressure toward rigid programming of these structures. individual variation of copuline production is consider- It indicates that the sphere of sexual behaviour was able, it distinguishes sexually mature from immature never so significant in the evolution of the Homininae females (Fox 1982). The fact that chimpanzee males in- as to require selection for any strictly defined type of spect the vagina with their fingers, which they later reproductive strategy in Homo. smell and lick, shows that olfactory communication in The pressure of the changing environment in human the chimpanzee is also relatively weak but that males evolution—climatic conditions involving the need to look for these stimuli (Nishida 1970, cited by Fox 1982). overcome various nutritional stresses, change in the di- Thus the weakening of olfactory signaling is not simply etary niche, and increased heat and later probably pawŁowski Loss of Oestrus and Concealed Ovulation 267 cold—was more significant in the process of hominiza- mental support by providing links between habitat tion than sexual selection and the often postulated quality, resource abundance, and sexual behavior (re- change in reproductive strategy. viewed in Andersson 1994). Rather than eliminating sexual selection, changes in resource abundance will af- fect the social and the genetic mating system and hence the associated social and sexual behavior. Comments ‘‘Cultural’’ explanations of human behavior erron- eously lead to the assumption that current variations in sexual behavior, mate preferences, and reproductive a. p. møller and b. sille´ n-tullberg1 success are cultural artifacts rather than examples of Laboratoire d’Ecologie, CNRS URA 258, Universite´ sexual selection in action. By ‘‘sexual selection’’ we Pierre et Marie Curie, Baˆ t. A. 7e`me e´tage, 7 quai St. mean nonrandom variation in mating success associ- Bernard, Case 237, F-75252 Paris Cedex 05, France ated with variation in one or more phenotypic charac- ([email protected])/Department of Zoology, ters. There is ample evidence for such variation in hu- University of Stockholm, S-10691 Stockholm, mans, with features such as symmetry and wealth being Sweden. 6xi98 associated with number of mates and sexual partners (e.g., Borgerhoff Mulder 1991, Thornhill and Gangestad Pawłowski correctly emphasizes that concealed ovula- 1994). Intense sexual selection is also associated with tion and nonreproductive sex are not unique to humans particular body odors, and the degree of female prefer- and that chimpanzee-like anogenital swellings are un- ence for these odors has been demonstrated to be related likely to have occurred in ancestral Hominidae or Ho- to proximity to ovulation (Gangestad and Thornhill mininae. However, his claim that direct selection of 1998). This preference is perceived entirely at a subcon- sexual behavior was absent in early Homininae seems scious level, and therefore any deliberate choice or po- unjustified. First, phylogenetic analyses suggest that licing activity influenced by culture is unlikely to have while concealed ovulation is likely to evolve in lineages generated it and its mere existence is evidence for with overtly polyandrous females, once evolved it strong current (and hence in all probability past) sexual seems to facilitate the evolution of social monogamy selection. Thus, it seems unlikely that the evolution of (Sille´n-Tullberg and Møller 1993). The evidence for sex- human sexual traits took place in a context devoid of ual behavior and social mating systems in hominids and sexual selection pressures. Although ovulation in hu- extant human societies fits this scenario, although mans may not be signaled visually as in many other pri- Pawłowski misses this point. Secondly, the claim of re- mates, there is compelling evidence that modern laxation in sexual selection seems unjustified given women are able to signal ovulation by changes in asym- current patterns of human sexual behavior. metry in soft body parts (Manning et al. 1996) and by While Pawłowski interprets intraspecific variation in changes in dress and behavior (directly related to sali- copulation frequency as a cultural phenomenon, such vary levels and hence stage in the menstrual variation is common throughout the animal kingdom cycle [K. Grammer, personal communication]). If phe- (Møller and Birkhead 1992, Birkhead and Møller 1998). notypic variation in these traits is associated with dif- An important determinant of sexual behavior is spatial ferences in mate choice or sexual behavior and if these and temporal variation in its costs and benefits. Accord- differences are partly controlled by heritable variation, ingly, within-pair copulation rates increase in social these recent findings provide further evidence for a cur- contexts where extra-pair copulations are frequent. Fur- rent role of sexual selection in shaping female reproduc- thermore, males often retaliate with copulation in re- tive strategies. sponse to presumed extra-pair copulation by a mate Pawłowski discusses long- versus short-distance sig- (Birkhead and Møller 1992), even among humans (Baker naling in humans. Multiple signals are common in and Bellis 1995). An increase in copulation frequency in many signaling systems; different phenotypic features Western societies may indeed be a cultural phenome- may be signaled by different signals, or a particular sig- non in that culture alters the conditions for extra-pair nal may give a partial indication of the individual’s copulations, thus altering the cost/benefit ratio for overall phenotypic character (Møller and Pomiankow- within-pair copulations. ski 1993). Such signals may interact in a number of Pawłowski neglects the role of sexual selection in the ways and provide information about different features evolution of human sexual behavior. Theory predicts at different distances. Speculation about the role of dif- that the ecology and hence the habitats chosen by indi- ferent signaling systems must await studies of how viduals of a particular species affect the social mating these systems interact and the distances at which sig- system and hence sexual selection (Emlen and Oring nals are perceived. 1977). This long-standing tradition in behavioral ecol- In conclusion, there is ample evidence to suggest that ogy has gained considerable observational and experi- sexual selection currently acts on phenotypic variation in humans, although it remains undetermined whether 1. K. Grammer kindly provided unpublished information. APM such selection will result in microevolutionary change. was supported by a start-up grant (atipe blanche) from the CNRS; We believe that progress in the understanding of loss of BST was supported by the Swedish Natural Science Research. estrus and concealed ovulation will come from detailed 268 current anthropology Volume 40, Number 3, June 1999 studies of intraspecific phenotypic variation and its served distribution of coitus across the menstrual cycle causes and reproductive consequences. and (2) the widespread misidentification of the timing of the fertile period. Although Pawłowski is skeptical of the evidence for beverly i. strassmann concealed ovulation in humans, he nonetheless sug- Department of Anthropology, University of Michigan, gests that estrus is absent in many other primate spe- Ann Arbor, Mich, 48109, U.S.A. ([email protected]). cies. Phylogenetic analyses suggest that sexual swell- 13 x 98 ings were independently lost in primates about 6 times (Strassmann 1996b, c)or8–11 times (Sille´n-Tullberg Pawłowski states that ‘‘field data on all the nonhuman and Møller 1993). However, the absence of swellings primates indicate the highest frequency of sexual activ- does not constitute the absence of estrus unless the be- ity in the ovulatory phase of the cycle.’’ Yet he ques- havioral and olfactory cues that signal ovulation are tions the ‘‘assumption that the absence of oestrus and also absent. To the best of my knowledge, in all nonhu- concealed ovulation in Homo are exceptional’’ and con- man primate species the highest frequency of copula- tends that the ‘‘absence of oestrus is quite frequent in tions occurs around the time of ovulation—implying the primate order.’’ Further, he concludes, ‘‘Research on that in nonhuman primates estrus signals remain human sexual behavior has demonstrated fluctuations present. in proceptivity and attractiveness approximating those Although the 18th-century French philosopher Mon- in the chimpanzee.’’ How do these statements square tesquieu was not technically correct when he wrote, with the evidence? ‘‘Man is the only animal who eats when he is not hun- Studies of the common chimpanzee (Pan troglodytes) gry, drinks when he is not thirsty, and makes love in all report that 94% to 96% of all copulations took place seasons,’’ his emphasis was in the right direction. Some during or around the period of maximal swelling (re- primates copulate throughout the calendar year, but the viewed in Takahata, Ihobe, and Idani 1996). Early re- loss of estrus is apparently unique to humans and re- ports on bonobos (P. paniscus) emphasized that copula- quires explanation. Because estrus conveys such repro- tions occurred throughout the cycle (Savage-Rumbaugh ductively significant information, it is hard to see how and Wilkerson 1978), but a more recent study by Furui- it could be lost as a mere side effect of ecological and chi (1987) reports that 82% of copulations took place cultural factors. A trait that enables males (and other when swellings were maximal. This finding was rein- females) to detect the fertile period does not seem like forced by a study of two additional groups of bonobos one to which selection would have been indifferent. In- in which 77% and 67% of copulations occurred during stead it seems more plausible that changes emerged in maximal swelling (Takahata, Ihobe, and Idani 1996). In the costs and benefits of signaling ovulation. Two de- humans there is no such pronounced increase in copula- cades have elapsed since debate began on the evolution tion around the time of ovulation. Summarizing the lit- of concealed ovulation (e.g., Alexander and Noonan erature, Hill (1988) concluded that 10 of 12 studies 1979). Data to resolve this debate will be difficult or im- found a postmenstrual increase in the probability of possible to obtain, but I venture the prediction that copulation, 8 of 12 showed a luteal decrease, 4 of 12 hypotheses based on sexual selection will remain at the showed a premenstrual increase, and 6 of 12 showed a core of future discussions. midcycle peak (though not an exclusive one). The hy- pothesis that humans display a chimpanzee-like prefer- ence for copulation around the time of ovulation was not supported. Prior to the 20th century, many gynecol- jan strzałko ogists believed that ovulation coincided with menstrua- Institute of Anthropology, Adam Mickiewicz tion (reviewed in Strassmann 1996a), and reproductive University, Poznan´ , Poland. 20 xi 98 biologists (e.g., Marshall 1910) confounded menstrual bleeding in women with pre-estrus bleeding in dogs. The sphere of human sexual behaviour, guarded in our Among the Dogon of Mali, people use the same term culture by numerous taboos, is rather readily stereo- for menstruation in women as for estrus in domestic an- typed even in anthropology. The life of the stereotypes imals. They recognize that dogs and cows are most fer- formed in this field is very long, especially when they tile just after bleeding has stopped and assume that the are supported by the conviction of the unique position same is true for women; husbands therefore often insist and role of our species in . Pawłowski rightly on copulation immediately after a woman returns home questions one of these—the significance of change in from the menstrual hut (Strassmann 1996a). Rather sexual behaviour and sexual signaling for hominisation. than being an isolated example, the Dogon view appears Because of the vastness of the problem he analyses only to have been cross-culturally widespread. In the Stan- one of its aspects, one particularly deeply rooted in an- dard Sample of 186 societies, the prevailing belief was thropogenetic interpretations—the notion of the con- that conception occurred immediately after menstrua- stant sexual receptivity of females (including so-called tion (Strassmann 1996a; see also Paige and Paige 1981). concealed ovulation). Far from limiting himself to ques- Thus, Pawłowski’s view that ovulation in women is not tioning the stereotype, he advances his own proposal for truly concealed is hard to reconcile with both (1) the ob- the interpretation of evolutionary changes resulting in pawŁowski Loss of Oestrus and Concealed Ovulation 269 the present condition of human beings with regard to thropologists though practised by few. He points to the above-mentioned traits. the incorrect division of the families Pongidae and Exposition of the case on the constant receptivity of Hominidae and appropriately recommends a separate females related to the lack of oestrus and symptomless Homininae taxon (subfamily) for the australopithecines ovulation is in fact a relatively easy task. Pawłowski and humans. has been able to draw abundantly upon the argumenta- tion presented by the authors of numerous contradic- tory conceptions. In particular, he has tried to demon- linda wolfe strate the falsity of the belief in the uniqueness of Department of Sociology and Anthropology, East constant receptivity in women, this phenomenon, like Carolina University, Greenville, N.C. 27858-4353, the loss of the symptoms of ovulation, being observed U.S.A. 5xi98 in at least a few other primates. He has also attempted to show that it is impossible to find a straightforward There is much positive to be said about this article. dependency between this feature of the sexual cycle and Pawłowski argues that modern humans share many the increase in informational complexity (socialisation) characteristics of their reproductive biology and sexual within a group. Finally, he has sought to show that in behavior with the other anthropoid primates. He sup- fact women’s receptivity cannot be regarded as abso- ports his argument by pointing out that for humans and lutely constant and their ovulation is not entirely the anthropoid primates lacking a sexual swelling (that symptomless. is, those with concealed ovulation) the act of mating His work is, however, based on the published litera- may or may not be timed to ovulation. Moreover, he ture, and I assume that he has not dealt with the socio- argues convincingly that the extreme sexual swellings biological or ethological issues on the experimental of chimpanzees and bonobos arose after the Paninae/ level. It is worth remembering that, even though no Homininae split. Likewise, his review of the literature hypotheses are tested, this does not affect the reliability suggests that human sexual behavior is not completely of the account. The numerical weight of the materials, independent of the hormonal fluctuations of the men- one of the parameters of the reliability of experimental strual cycle and follows a pattern similar to that found research, is represented in literature-based work by the in other anthropoids—in other words, that the overall number of the publications referred to, and this number pattern of human sexual behavior is not unique among is undoubtedly sufficient. At the same time, whereas the anthropoid primates. the number of measurements taken in an experiment Taking into account the similar behaviors of human (usually) indicates high reliability (repetitiveness), the and other anthropoids, Pawłowski reasons that human situation with a set of published sources may be en- reproductive biology and sexual behavior are not the tirely different—especially when the works come from product of recent sexual selection or a new reproductive the methodological fringe as in my opinion do many strategy. I concur. Alternatively, he argues that climatic works in the field of human . In this context, and nutritional stresses were the significant forces in the persuasiveness of table 1 is very limited. Pawłowski the hominization process. He does not, however, ad- implies that it is difficult to interpret the results of re- dress the question of the causal factors involved in the search conducted on contemporary American or Euro- changes from the basic mammalian reproductive pat- pean women because of the great many cultural factors tern to the sexual behavior of the anthropoid primates. that can only be partly controlled. However, he readily This pattern of continuous sexual receptivity with accepts the results of research on ‘‘hunter-gatherer peo- fluctuations in proceptivity and attractiveness over the ples,’’ which in my view are not lacking in cultural fac- course of the menstrual cycle is typical of the anthro- tors (beyond control in the research) that affect the poid primates including humans. Because this pattern rhythm of sexual behaviour of their members. What is of sexual behavior is widespread among the anthropoid more important, he does not comment on the fact that, primates, it probably evolved early in their evolutionary although the symptoms of ovulation in women (and in history, perhaps as early as the Oligocene. Compulsive several other primates) are concealed, Homo is the only sociality, intense social relationships, increased brain species with a clearly marked point of the cycle oppo- size, and greater behavioral flexibility are among the site to ovulation, namely, menorrhoea. In speaking factors that may have helped to alter the basic mamma- about constant receptivity we usually do not mean re- lian reproductive pattern. ceptivity during menstruation. The question of the evolution of the sexual behavior Despite these objections, I am inclined to agree with of the anthropoid primates is, of course, one of the more Pawłowski that the (relative) symptomlessness of ovu- interesting problems of primate evolution. An under- lation and the specific character of sexual behaviour are standing of the evolution of human sexual behavior will a consequence rather than a cause of significant changes come only as we expand our knowledge of the relation- giving direction to the process of hominisation. He of- ship between receptivity, proceptivity, attractiveness, fers a taxonomic proposal that could be the subject of and sexual activity in humans and the other anthropoid a separate study in itself. His stand on the taxonomy primates. The endeavor to understand primate sexual of the Hominidae is absolutely right, in my opinion, behavior requires interdisciplinary research, and Paw- expressing the view supported by the majority of an- łowski is to be commended for bringing together the lit- 270 current anthropology Volume 40, Number 3, June 1999 erature of several different disciplines. Future attempts tion, these tendencies confound Strassmann’s claim to understand human and nonhuman primate sexual that humans are unique in lacking oestrus. behavior will require a similar interdisciplinary ap- I agree with Møller and Sille´n-Tullberg that intraspe- proach. cific variation in copulation frequency is common in the animal kingdom. I wanted to show how some cul- tural factors can influence this variation as well. The main variation is of course biological, and this is why I emphasized the fact that reproductive behaviour due to Reply sexual selection may become more important in terms of general fitness when other (natural) selective pres- sures on individuals’ fitness are relaxed. Becoming suc- bogusław pawłowski cessful in avoiding predators, acquiring adaptations to Wrocław, Poland. 21i99 variable climatic conditions, or being very effective in food extraction in harsh (i.e., resource-poor) environ- I thank the commentators for their responses and in- ments leaves more room for the discriminative role of sightful comments on some points of my paper. There sexuality (e.g., in the stages of mental evolution in hom- is little consistency among them, and some of their inines when some relaxation of natural selection proba- opinions are contradictory to those of others (e.g., the bly occurred). Møller and Sille´n-Tullberg are right that recognition of the signs of ovulation in women by copulation rate increases in social contexts where ex- Møller and Sille´n-Tullberg and the denial of any such trapair copulations are frequent. This explains why sex- signs by Strassmann). I am pleased with the general ual activity is not as frequent in single-male (e.g., agreement on my main points of Strzałko and Wolfe and gorilla) or monogamous (e.g., gibbon) social structures, glad to have the opportunity to take up the challenges where is negligible, as in chimpan- by Møller and Sille´n-Tullberg and by Strassmann. zees or macaques. Nevertheless, the copulation rate in Møller and Sille´n-Tullberg agree that ‘‘chimpanzee- Western societies is determined not only by the altered like anogenital swellings are unlikely to have occurred conditions for extrapair copulations, as Møller and Sil- in ancestral Hominidae or Homininae’’ and recognize le´n-Tullberg suggest, but also by hormone levels due to that ovulation in humans is signaled nonvisually. Both various factors (e.g., the ecological and economic condi- of these points undermine their critiques based on phy- tions I mentioned). logenetic analyses of visually concealed ovulation (not Møller and Sille´n-Tullberg seem to have overlooked to mention that there is no consensus on analyses of my suggestion that bipedality, olfactory communica- this trait and that there are primates that do not fit tion (in hot, open environments), a prolonged period of them). I doubt that this argument is good enough to development, and other biological (N.B.: not cultural) allow conclusions about the operation of sexual selec- traits may have been important in the evolution of hu- tion on the traits in question in our ancestors. There is man sexual behaviour. I have used cultural data to show still considerable debate about ‘‘sexual behaviour and instead why (1) in some cases the results of research on social mating systems in hominids,’’ and therefore I do sexual behaviour across the female cycle do not fit the not know either what other evidence or what scenario expected fluctuation rates and (2) we should be careful these models are supposed to fit. Møller and Sille´n-Tull- about drawing conclusions and suggesting evolutionary berg also take for granted that Homo sapiens is monoga- mechanisms for hominines or early Homo on the basis mous. I am afraid that in the light of morphological of data from one or two particular cultures. (sexual dimorphism in body size), ethnographic (the ma- Contrary to their suggestion, I do not assume that jority of societies are polygynous), and psychological ‘‘current variations in sexual behavior, mate prefer- (men desire to have more partners and adultery is fre- ences, and reproductive success are cultural artifacts.’’ quent in both sexes) evidence even this assumption I did not deny the existence of sexual selection on such does not seem so obvious. features as body symmetry or general physical attrac- The variability of human reproductive strategies in tiveness (for example, waist-to-hip ratio) and certain contemporary human populations (monogamous, po- psychological traits influenced by sex. Rather, my aim lygynous, polyandrous, and polygynandrous [see Daly was to undermine the position of writers such as Parker and Wilson 1983]) indicates great flexibility. This may (1987), who, in postulating mechanisms of human evo- mean that, contrary to the opinions of some writers, se- lution, have overestimated the role of sexual selec- lection on reproductive behaviour could not have been tion—particularly when their main arguments are very strong or rigid in human evolution. There is also based on the assumption that the loss of oestrus and an increasing tendency among the primate taxa towards concealed ovulation are uniquely human. less rigid ovarian hormonal control over sexual recep- I agree with Møller and Sille´n-Tullberg about the im- tivity (Dixson 1998:331). This general tendency in pri- portance of unconscious olfactory communication, mates to lose oestrus without any corresponding reduc- which influences the frequency of sexual behaviour and tion in the variety of mating systems represents a thus increases the probability of fertilization. Olfaction problem for Møller and Sille´n-Tullberg’s idea of specific still performs a reproductive function, though I doubt sexual selection pressure in human evolution. In addi- that it is in the ‘‘intense [my emphasis] sexual selection pawŁowski Loss of Oestrus and Concealed Ovulation 271

. . . associated with particular body odors’’ as Møller and highest rate of copulation is observed at midcycle in the Sille´n-Tullberg (citing Gangsted and Thornhill 1998) majority of anthropoids. write. My claim does not depend entirely on the mask- Strassmann cites copulation percentages during the ing of natural odours and reduced conditioning to such period of maximal swelling for chimpanzees and bo- odours in the very early stages of life in our culture, nobos from Takahata, Ihobe, and Idani (1996). Copula- both of which lessen the functionality of the informa- tion rate during tumescence ranges from only 62–65% tion they convey. Apart from information about the fer- (Wallis 1982, Coe et al. 1979) in chimpanzees to 82% tile period of the menstrual cycle and some clues about (Furuichi 1987) in bonobos. Wallis (1986, cited in Wallis genetic distance (e.g., Wedekind et al. 1995), odours do and Englander-Golden 1992) found that chimpanzee fe- not convey much information about the partner’s value male receptivity did not vary with cycle phase. The re- that would serve as a measure of potential reproductive sults may vary with ecological conditions (e.g., the dif- success. The physical attractiveness (appearance) or age ferent results for wild and captive chimpanzees may, as of a woman and the wealth, status, or intelligence of the I have suggested, be the effect of the relaxation of natu- man seem more important and valuable information for ral selective pressures in captivity). the opposite sex in long-term mate-choice strategies. In We should remember that the period of maximum addition, we should not forget that sexual preferences swelling can constitute as much as 40% of the cycle for have evolutionary value only when positively corre- chimpanzees and 47% for bonobos (Takahata, Ihobe, lated with reproductive success. and Idani 1996), and it is much longer than the periovu- Møller and Sille´n-Tullberg emphasize the ‘‘current latory period, approximating the entire length of the role of sexual selection in shaping female reproductive proliferative and ovulatory phases in humans. From the strategies,’’ but when we speculate about the past we data we have on sexual activity in humans—for exam- must keep in mind that many other traits that have ple, in addition to the earlier-cited results of research by emerged in human evolution may have influenced hu- Harvey (1987) and Matteo and Rissman (1984), Bancroft man reproduction—perhaps even more than one could et al.’s (1983) report of mid-proliferative-phase weekly expect solely by means of sexual selection. In many pri- frequencies of ca. 2.8 compared with ca. 1.9 in the later mates that lack visual signals of ovulation there are phases and 1.3 in the early proliferative phase—allow some vestiges of a swelling either in pregnancy (e.g., in us to estimate that probably an average of more than orang-utans) or in adolescence (e.g., in patas monkeys, 50% (or even 60%) of sexual activity takes place in gorillas, rhesus monkeys, and stump-tailed or Japanese these two phases (therefore in about 40% of the cycle). macaques) (Anderson and Bielert 1994). The lack of ob- All of these results were obtained despite the many dis- vious vestiges in the human female may mean either turbing and novel factors in Western society which can that our ancestors never had this swelling or that the influence sexual behaviour. Unfortunately, we have no disappearance of the swelling may have an important detailed data that might allow the calculation of per- physiomorphological basis specific to this line (e.g., bi- centages of sexual activity across the cycle in !Kung San pedality, fur loss, and/or subcutaneous fat tissue in- women, but I think it is justifiable to assume wider crease). fluctuations in all the human ancestors. For the bo- I concur with Møller and Sille´n-Tullberg that it is un- nobos in group E2, 67% of copulations took place dur- likely that human evolution was devoid of sexual selec- ing 39% of the cycle (Takahata, Ihobe, and Idani 1996); tion pressures. The problem is on which traits it it seems that this species does not have a true oestrus, worked, whether this selection was in some way unique as this distribution is not dissimilar to that of sexual or different from the sexual selection in other primates activity in some humans. and calls for special explanation, and whether this se- The major problem posed by the data from Mahale— lection was responsible for the hominization process. where 94% of copulations took place during the period Even if the loss of oestrus and the way in which ovula- of maximal swelling—is that the adult sex ratio was tion is (or is not) signaled were really unique for humans highly biased towards females (10:39). Given that, ac- (and they do not seem to be), we cannot rule out the cording to Takahata, Ihobe, and Idani (1996), there was possibility that the lack of continuity of these traits no ovulatory synchrony, one would expect males to among the anthropoids is just a side effect of other have preferred the most attractive females (i.e., those novel and/or unusual (for primates) traits that emerged with maximal swellings). This skewed sex ratio also ex- in the evolution of the hominines. plains why (1) 80% of conceptions at Mahale occurred Strassmann questions that primates other than hu- in opportunistic matings (and not at all in consortships, mans have lost oestrus. According to some writers (e.g., as at Gombe [Tutin 1979]) and (2), contrary to the re- Chalmers 1979; Dixson 1998; Martin 1990, 1992; Wolfe sults of other studies, at Mahale adult females often 1991) and in line with the original definition of oestrus took the initiative in copulation. by Heape (1900, cited in Dixson 1998), the existence of High female proceptivity was linked with intense oestrus in anthropoids is rather dubious. Indeed, Martin female-female competition over access to males. The (1990) has proposed calling oestrus and the menstrual adult sex ratio was also skewed in the case of two cycle ‘‘the female cycle.’’ Therefore there is nothing groups of bonobos in Takahata, Ihobe, and Idani’s data contradictory in my statement about the lack of hu- (ranging in different years from 7:9 to 9:13). In all man-specificity of this trait despite the fact that the groups, then, males were in a relatively good position 272 current anthropology Volume 40, Number 3, June 1999 and were more prone to copulate only with females of ovulation, however, because the fluctuation in sexual with maximal swellings. Very high percentages of sex- indicators and spontaneous sexual activity are suffi- ual activity in the period of maximal swelling in chim- cient to signal the fertile phase of the cycle. There are panzees may also be due to the fact that in this species other signs as well (see, beyond those cited in my paper, the increase in the copulation rate in this phase is much the comment by Møller and Sille´n-Tullberg), and one greater than in humans (50 copulations per day for a can add to these the pain at the time of ovulation in chimpanzee female [Wrangham 1993]). This may mean some women). In all of human evolution, as in that of that there are no great differences between chimpanzees other animals, it is not knowledge that facilitates the and humans in terms of copulation rate in other phases reproductive efficacy of sexual behaviour but the ste- of the female cycle and only much more pronounced roid hormones. Apart from refraining from sex during sexual activity (e.g., due to the intense sperm competi- menstruation, one possible ultimate reason for the pref- tion between males) in the period of maximal swelling erence for women in the early rather than the later pro- in chimpanzees. Bonobos mate at lower intensity than liferative phase in some societies and in harems (Betzig chimpanzees and have less than 70% of copulations in 1992, Einon 1998) could be selection for women with the period of maximal swelling. shorter cycles (and thereby those who ovulate fre- The other problem with the chimpanzee data is the quently and are in better health) and thus an increase age structure of the group. Including the sexual activity in reproductive success for men who choose to fertilize of adults, subadults, or even juveniles may produce dif- such women. I think that Strassmann would agree that ferent degrees of fluctuation across the female cycle. copulation in the early proliferative phase offers more The more indiscriminate (more equally distributed) sex- opportunity for conception to occur than copulation in ual activity across the female cycle in many subadult the relatively long postovulatory phases. Research on primates prompted me to suggest that human sexuality the moment of conception across the cycle confirms the may be the result of the prolonged period of the develop- possibility of conception for at least two-thirds of the ment in ontogeny and/or ‘‘behavioural neoteny.’’ Pro- cycle, with the peak between the 8th and the 14th day longed development is linked to increase in brain size, (Martin 1992). Perhaps we concentrate too much on the which may mean that some differences in sexual behav- evolutionary meaning of concealed ovulation rather iour between humans and alloprimates are at least to than, as Burt (1992) suggests, on why conspicuous ad- some extent side effects of the encephalization process vertisements of ovulation have developed in some pri- in the course of human evolution. mates. Strassmann is unhappy with the chimpanzee as a ref- I agree with Strzałko that there are cultural factors in- erence for humans. Perhaps some macaques (M. fascicu- fluencing sexual behaviour even in hunter-gatherer so- laris or M. arctoides) or vervet monkeys (Cercopithecus cieties, but they are still better living societies to model aethiops), which do not have so pronounced an increase our ancestors’ sexual behaviour on than Western soci- in copulation rate in midcycle, would be a better model ety. Menstruation and its evolution were not the sub- for the distribution of sexual activity across the female ject of my paper, but Strzałko wrongly assumes that the cycle in humans. My comparison of humans with chim- menstruation is uniquely human. It is covert in prosim- panzees or macaques is based on the general pattern of ians and platyrrhines but is very marked (i.e., with copi- fluctuation of sexual activity across the female cycle ous vaginal bleeding that is highly visible) in many cat- rather than its degree. As I have said, the human distri- arrhines. Does the human female bleed more during bution of sexual activity may be flatter than in other menstruation than Old World nonhuman primates? anthropoids, but this may not be a qualitative differ- Here again we have a problem with quantitative differ- ence. The question is whether one can speculate about ence. Studies show (Dixson 1998:273) that after multi- unusual sexual selection pressure on humans during ple nonconception cycles many female primates have their evolution on the basis of quantitative differences heavier . Frequent and copious menstrua- alone. Similar differences can be found between some tion in women may simply be a reflection of abnormal species of macaque, and it does not seem to alter their physiology (adult females are pregnant or lactating most social structure very much. The general question would of the time), and, as Dixson states, this does not seem be what degree of quantitative difference would call for to be relevant to evolutionary questions. explanation in terms of specific, direct selection pres- Wolfe rightly points out that we need to think more sure in the course of human evolution. A more fruitful about the general trend of receptivity in anthropoid pri- approach, as Wolfe suggests, would be to seek to iden- mates, but first we need to admit that humans follow tify the mechanisms underlying the anthropoids’ ten- the general primate trend and are not the exception. It dency to lose oestrus. is not going to be an easy task, but the research direc- Strassmann’s comment on my scepticism about con- tion that Wolfe indicates could be very promising for cealed ovulation in humans and my claim that oestrus the understanding of the evolution of human and non- is absent in many primates shows that she does not ap- human primate sexuality. On the basis of the greater preciate the fact that lost oestrus need not be accompa- variability of gestation time in the anthropoids, Martin nied by concealed ovulation. She supports her claim (1992) suggests that the loss of oestrus and the distribu- that there are no signs of ovulation in the human female tion of sexual activity throughout the female cycle in by citing cultural misidentification of the time of ovula- many Old World primates could be explained by more tion. Humans do not need to have conscious knowledge vital spermatozoa, longer ovulation, or more frequent pawŁowski Loss of Oestrus and Concealed Ovulation 273

multiple ovulation. Another possible explanation sperm competition? Data for humans. Animal Behaviour 40: might be some new element in addition to the many 997–99. ecological factors that determine sexual behaviour. One be nsh oo f, l., an d r. t ho rnh il l. 1979. The evolution of monogamy and loss of estrus in humans. Journal of Social and possible candidate for such an element is the relative Biological Structures 2:95–106. increase in size of the brain or some part of it (e.g., the be tzig, l. 1992. Roman polygyny. Ethology and neocortex) and more complex control over the hor- 13:309–49. mones involved in sexual behaviour. In primates living bi rkhe ad, t. r., an d a. p. mø lle r. 1992. Sperm competi- tion in birds. London: Academic Press. [apm, bs] in multimale groups with higher neocortex ratios, the ———. Editors. 1998. Sperm competition and sexual selection. correlation between male rank and mating success is London: Academic Press. 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Institutions

At a meeting of the Permanent Council of the Interna- the use of replicas of hominid fossils, rather than the tional Association for the Study of Human Paleontology original hominid fossils, for public display to promote in Sun City, South Africa, on July 3, 1998, concern was public awareness and understanding of human evolu- expressed about a proposal to send certain original Afri- tion. can hominid fossils to an American museum for dis- 2. We strongly recommend that original hominid fos- play. The matter was discussed and the following reso- sils should not be transported beyond the country of ori- lution was adopted: gin unless there are compelling scientific reasons which 1. Recognising that hominid fossils are an irreplace- must include the demonstration that the proposed in- able component of world heritage, we, the members of vestigations cannot proceed in the foreseeable future in the Permanent Council of the International Association the country of origin. for the Study of Human Paleontology, strongly support