Sexual Selection, , and Concealed in

Beverly I. Strassmann

Changes in the social structure of early humans greatly INTRODUCTION enhanced the potential for paternal care to contribute to success. Selection therefore favored females In the superfamily Hominoidea, females who mated with more paternal males. Since paternal are unique in that they may be sexually receptive care limits mating effort, males least successful as po- lygynists would have the most to gain by paternal be- at any time of their cycle and do not exhibit a havior, while the successful polygynists would gain least. phase of pronounced physiological or behavioral may have evolved because it pro- estrous cues that overtly signal ovulation to moted the paternal tendencies of the less polygynous themselves or to males (Butler, 1974; Alexander males who advanced female the and Noonan, 1979; Benshoof and Thornhill, most. Since the offspring of indulgent males would have 1979; Burley, 1979; Hrdy, 1979; Symons, 1979). a competitive advantage over the offspring of more po- Thus, in the evolutionary line leading to humans, lygynous males, and females revealing the time of ovu- there clearly has been selection to conceal ovu- lation would become increasingly scarce, all males would lation. Understanding the selective background eventually pursue a reproductive strategy emphasizing that led to the concealment of ovulation in hu- paternal effort over mating effort. mans could improve our understanding of inter- In nonhuman the most polygynous males mate selectively with females who are likely to be ovu- actions between the sexes and provide insight lating. Sueh males would probably not mate with females helpful in improving contraceptive methods. The having dhninished cues to the time of ovulation. The present paper will (1) review five recent hy- more paternally prone males could therefore consort potheses on the evolution of concealed ovulation with these females and experience a high confidence of and (2) employ the theory of sexual selection to paternity. Another characteristic of nonhuman primates modify the scenario proposed by Alexander and is that the most successful polygynists tend to have a Noonan (1979). The resulting hypothesis is sup- high dominance rank. Thus, female hominlds who mated ported by behaviors of primates, and it is con- with more paternal males may have sacrlflced having sistent with a possible explanation of the sub- offspring with some of the gene& advantages that con- tribute to dominance. However, subconscious physiolog- conscious physiological and psychological ical and psychological correlates of ovulation in humans correlates of human ovulation. may have tempted females to exploit infrequent, low- risk opportunities to mate outside the pair-bond with males of superior genetic . These correlates may also promote conception irrespective of mating partner, PREVIOUS HYPOTHESES or they may have helped females avoid rape. Burley (1979) proposes that concealed ovulation Key Words: Concealed ovulation; Dominance rank; evolved to counteract a tendency of hominid fe- Estrus; Paternal care; Polygyny; Reproductive stra- tegies; Sexual selection. males to deliberately avoid conception. She ar- gues that the motivations for this behavior, such as fear of death, fear of pain, and the inconven- Received April 3, 1980;accepted October 16, 1980 ience of having children, stem from the evolution Address reprint requests to: Beverly I. Strassmann, c/o Dept. of Entomology, Comstock Hall, Cornell University, of a large cerebrum. However, if a large cere- Ithaca, NY 14853. brum were responsible for such dramatically

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Ethology and Sociobiology 2: 31-40 (1981) 0 Elsevier North Holland, Inc.. 1981 0162-3095/81/0100031-10$02.50 52 Vanderbilt Ave., New York, New York 10017 32 Beverly I. Strassmann nonadaptive behavior its disadvantages would guishing humans from other primates. She may probably have outweighed its advantages. More- mean that concealed ovulation evolved in a com- over, studies of nonhuman primates make it mon ancestor to the Hominoidea (great and doubtful that females in obvious estrus could humans). At such an early stage in evolution, have thwarted attempts by males to impregnate prehominids might not yet have become partic- them. Selection for concealed ovulation as a ularly cooperative within groups. This idea is means of promoting conception therefore would implausible since humans are the only members not have occurred. Burley’s conclusion that of the superfamily Hominoidea who have con- there is an apparent lack of female initiation of cealed ovulation. copulation during ovulation is contradicted by Even if cooperation within groups is strong, a study reporting an ovulatory peak in female- it could be argued that concealed ovulation initiated sex (Adams et al., 1978). Adams et al. evolved to counteract practiced by attribute the conflicting results of earlier studies males from outside the group. Evidence provided (e.g., McCance et al., 1937; James, 1971; Spitz by Bygott (1979) indicates that et al., 1975) to measures of sexual activity in (Pan troglod.ytytrs) of the same troop have few which the ovulatory rise in female-initiated cop- aggressive encounters over females, while in- ulations is masked by male-initiated copulations. tergroup competition for females is fierce and Hrdy (1979) suggests that concealed ovula- sometimes involves infanticide. Similarly, infan- tion evolved among prehominid females as a ticide among the Yanoama is often associated means of confusing paternity so that males with the exchange of women in intercommunity would not be able to selectively kill the offspring warfare (Biocca, 1969). However, when infan- of other males. This model may explain sham ticide is practiced on the already born to estrus in Hanuman langurs (Presbytis ~ntelus) recruited into a different group, males but does not fit the evidence on prehominid so- of the new troop may be quite certain they did cial structure. The primates from whom humans not sire the infants. In this situation, the evo- evolved probably experienced strong competi- lution of concealed ovulation would only benefit tion between groups, thus enhancing unity and females who switched groups early in pregnancy cooperation within groups. Selection for coop- before their condition could be detected by erative hunting and predator defense would also males. It is, therefore, not surprising that con- have reinforced group solidarity (e.g., Alex- cealed ovulation has not evolved in chimpan- ander, 1974). If males in a troop gained by co- zees. These arguments imply that concealed operating with each other they would not have ovulation evolved in humans for a reason other profited from killing each other’s offspring. As than intergroup infanticide. Such infanticide Hrdy points out, in Savannah (Papio would, however, increase the importance of pa- c~nocephnlus) the males cooperate in predator ternal care; this could have been a precipitating defense and females have not evolved concealed factor in the evolution of concealed ovulation ovulation. According to Hrdy, “any male who (Alexander and Noonan, 1979). killed offspring belonging to a male still present Symons (1979) offers two scenarios to explain in the troop would reduce the stake that male the loss of estrus in humans. In one, humans had in risking his to defend the troop. Hence live in promiscuous polygynous bands and males all infants in a troop containing an infanticidal give meat to females in exchange for sex. Ac- male (including his own) would have been less cording to Symons, this practice caused females likely to survive.” Moreover, in an affiliative to prolong their stage of sexual attractiveness. troop, relatives and consorts of mothers would However, males who mated only with females help them defend their infants from attacking in true estrus would have been selected for rel- males (Smuts, in preparation, cited in Hrdy, ative to males who mated with females in either 1979). Bygott (1979) asserts that exaggerated true or sham estrus. Unless one assumes that over access to females will be pun- such discriminating males were extremely scarce. ished, since selfish males will not be able to par- it is questionable whether females who pro- ticipate in beneficial coalitions. longed estrus would have been given more meat Hrdy claims that continuous receptivity was and thus been favored by selection. part of the physiological heritage that prehom- In another scenario, Symons (1979) and Ben- inid females brought to the new lifestyle, distin- shoof and Thornhill (1979) suggest that con- Concealed Ovulation in Humans 33 cealed ovulation evolved to facilitate cuckoldry. of the hypothesis advanced in this paper. Yet The authors assert that females who did not ad- the evolutionary steps they propose are differ- vertise ovulation would have minimized the ca- ent. They suggest that through concealing ovu- pacity of their mates to monitor their reproduc- lation females forced desirable males into con- tive cycles and guard them during ovulation. If sort relationships long enough to decrease the at the time concealed ovulation evolved the males’ chances of success in securing other mat- human breeding system was monogamous or ings. The confidence of paternity of these males, harem polygynous (and females sometimes had according to Alexander and Noonan, was si- access to males who were genetically superior multaneously increased because potential com- to their mates), the cuckoldry scenario is cred- petitors no longer knew when females were ible. However, it is doubtful that females would ovulating. evolve induced ovulation or another trait that Their hypothesis implies that the highest would perfect their ability to cuckold males. quality females would be in demand by the high- Otherwise their mates would have such low con- est quality males and would enter into prolonged fidence of paternity that selection would dim- consortships with these males before subordi- inish their paternal care-whether or not males nate females and males would enter into con- discovered infidelities. sortships.’ It seems more likely that males most Alexander and Noonan’s hypothesis regard- successful as polygynists wotdd be the last to ing the evolution of concealed ovulation is based increase their paternal care, not the first. on the following assumptions: (1) At the time In order for high ranking males to abandon ovulation became concealed human was their successful polygynous strategy and in- polygynous and consisted of multimale bands. crease their paternal investment, differentials in Several studies link early humans with this social female quality would have to be remarkably system (Lee and DeVore, 1968; Jolly, 1972; steep. The relevant sample sizes are small, but Alexander et al., 1979; Brace, 1979; Campbell, some studies of nonhuman primates seem to find 1979). (2) During this period in instances in which females differ markedly in paternal care became an increasingly important their attractiveness (Hausfater, 1975) or in their determinant of offspring success. The increasing reproductive success (Goodall, 1971), while oth- importance of paternal care, according to Alex- ers point toward more uniform female quality ander and Noonan, is associated with intergroup (e.g., Loy, 1971; Kaufmann, 1965). Further competition and the growth in group size and studies are needed to determine whether steep unity. These developments increased the com- differentials are likely to have existed among plexity of social interactions and aggravated ju- human females. In the absence of steep differ- venile disadvantages in experience and strength. entials, high ranking males who copulated around Therefore, parents who conveyed to their off- the most likely time of ovulation with females spring the knowledge and skills needed for making having a precise estrus would probably have the the best decisions in complex social situations highest reproductive success. outreproduced less instructive parents. Other In addition to reducing the number of estrous authors point out that conflicting selection for females with whom a male can mate, partici- bipedality, which favors a narrow pelvis, and pation in a consortship potentially has other dis- larger size, which favors a wide pelvis, could result in more altricial young whose would grow large after (e.g., Fox, 1972: ’ “The highest quality females fin terms of ability to bear Benshoof and Thornhill, 1979). The advantages and rear offspring, and, perhaps, to enhance their status or of a longer learning period could also promote other correlates of reproductive success), would be in demand altriciality (Washburn’ and Lancaster, 1967: by the highest quality males most prone to polygyny; such females could afford to prolong estrus longer than others with- Pfeiffer, 1972). The increasing altriciality of out risk of desertion by the male. Low quality females would human young would further enhance the advan- be at least partially excluded from mating with the highest tages of parternal care. quality males by this ploy. Competition for matings by lower Alexander and Noonan’s two initial assump- quality males would be reduced (because top quality males tions, as well as their important idea that con- are already committed), making concealment of ovulation ad- vantageous to low ranking females in securing at least some cealed ovulation evolved in the context of fe- for their offspring” (Alexander and Noonan. males securing paternal care, are an integral part 1979, p. 448). 34 Beverly I. Strassmann

advantages discussed by Hausfater (1975). He tween the sexes, females are usually a limiting postulates such negative consequences as re- resource to males (Bateman, 1948; Trivers, duced food intake resulting from the need for 1972). One consequence is a general tendency constant guarding of the female, and increased toward polygynous breeding systems in which exposure to aggression and harassment from there is great variance in reproductive success other males. In his study of yellow baboons among males. In their competition to secure suc- (Pupio cynocephalus), the first ranking adult cessful matings with females, conspecific males males mated and consorted primarily on the op- have evolved alternative strategies involving timal day for mating. Lower ranking adults con- both behavioral and morphological differences. sorted on as many potentially fertile cycle days For a recent review of alternative male strategies as possible. According to Hausfater, the strategy among several classes of see Cade of the first ranking males gives them a relatively (1979). high probability of impregnating females while This theoretical framework suggests a pos- minimizing the negative consequences of con- sible selective background for the evolution of sortship. concealed ovulation. If humans were polygyn- High ranking males who entered into con- ous at the time concealed ovulation evolved, sortships with females who prolonged estrus some males by definition would have had more would suffer the additional disadvantage of the success at securing matings resulting in preg- higher cost of high confidence of paternity. nancy. Studies of nonhuman primates indicate When males need to guard their mate only during that those males who secure the most matings the brief period of estrus, confidence of paternity around ovulation tend to be dominant while sub- is least expensive (Benshoof and Thornhill, ordinate males find seeking matings a costly en- 1979; Burley, 1979; Symons, 1979). If a male deavor with a lower probability of success (see guards a female continuously, he compromises Conaway and Koford, 1965; DeVore, 1965: his ability to hunt and carry out the other activ- Kaufmann, 1965; Lindburg, 1971; Loy, 1971: ities that are at least indirectly an important com- Hausfater, 1975). Those males who are least suc- ponent of paternal care. Although concealed cessful as polygynists would tend to expend ovulation would greatly reduce the probability greater paternal effort on the offspring that they of matings outside the pair-bond resulting in produced with a relatively limited number of fe- pregnancy, the following males would still at- males. In fact, their options for increasing their tempt such matings: unmated males, males with reproductive success would resemble those of pregnant mates, and other males as low cost females. The successful polygynists, on the con- opportunities arose. Since confidence of patern- trary, would tend to expend less paternal effort ity would be more expensive for high-ranking on each of the offspring of a larger number of males, it is unclear how concealed ovulation in females. This argument is based on the assump- Alexander and Noonan’s scheme could increase tion that time and energy spent on mating effort paternal investment. In view of the disadvan- will limit paternal effort (see Alexander and Bor- tages of consortships to dominant males, it is gia, 1979). Borgia (1979) formulates the similar necessary to add to Alexander and Noonan’s argument that males who are unlikely to be suc- scenario the condition that the first males to pro- cessful at securing matings because of their rel- long their consortships would probably be those atively low genetic fitness may enhance their having a low probability of securing matings. reproductive success by providing females and Moreover, the females with whom such males their young with material benefits. Of course, consorted would have to be sufficiently unat- greater paternal effort on the part of subordinate tractive to the polygynous males that their con- males would have to be associated with en- sorts would have a high confidence of paternity. hanced confidence of paternity, and it would have to be the best strategy for these males to pursue in terms of their overall life history. As the potential for paternal care to be a de- CONCEALED OVULATION AND MATE terminant of offspring success increased so as SELECTION to exceed the importance of the male’s genetic Due to anisogamy, which may be the ultimate assets which do not contribute to paternal care, source of differential be- those males least able to monopolize matings Concealed Ovulation in Humans 35

would have become the most desirable mates. quently solicited mounting from adolescents. These arguments suggest that concealed ovula- Since dominant males cue in on estrus signs and tion evolved because it favored the strategy of do not mate with females with partial swellings, the subordinate, more paternal males who pro- they might pass up opportunities to mate with moted female reproductive success the most. females who had begun to reduce their estrus Females sacrificed the genetic benefits offered signs, even though these females would be fer- by the high ranking males in exchange for the tile. This behavior would reflect an inability of more important paternal benefits offered by the males to distinguish between females un- lower ranking males. Borgia (1979) also arrives likely to be fertile and females concealing ovu- at the conclusion that females sometimes must lation. Low ranking males would probably mate compromise potential gain from either the ma- with females who dampened their estrus signs terial or the genetic benefits offered by males in because they mate with females having partial order to maximize reproductive success. swellings. How would the concealment of ovulation en- It is probable that at the time concealed ovu- hance the confidence of paternity of the subor- lation evolved all males including the dominant dinate males? Subordinate males could probably ones already wqre somewhat inclined to be pa- keep their consorts from copulating with other ternal-perhaps bnly through protecting past or low ranking males, but not from the high ranking present female c$sorts or their young. Such males. However, if females who concealed ovu- behavior is thought TO occur to some extent in lation were sufficiently unattractive to the high all the great apes (Mitchell, 1969) and would re- ranking males, their lower ranking consorts duce the time and energy available to the dom- would have a higher confidence of paternity. inant males to seek suboptimal matings. Domi- nant males would be especially disinclined to attempt copulations with females appearing su- Female Attractivity boptimal if these females were being vigorously Behaviors of nonhuman primates indicate that defended by their low ranking male consorts. females who concealed ovulation by gradually Since their matings with females appearing su- dampening their estrus signs might have been boptimal would be rare, dominant males would unattractive to the dominant males. Observa- not experience strong selection for the ability to tions of baboons, rhesus monkeys, and chim- distinguish between females concealing ovula- panzees reveal a strong degree of selectivity in tion and females unlikely to be fertile. The rare the mating of the dominant males. First ranking matings that would occur between dominant male yellow baboons do not mate on all the po- males and females concealing ovulation would tentially fertile days of a female’s cycle, but in- not diminish the paternal behavior of the fe- stead constrain their mating to the optimal day, males’ indulgent consorts because the latter sometimes even the optimal time of day (Haus- would have been copulating with the females fater, 1975). On the optimal day estrus signs such much more regularly and therefore would be as sexual swellings are most pronounced. In more likely to sire offspring. other studies of baboons (Papio w-sinus and P. In nonhumans there is a close correlation am&is) and (Macaca mulatta), it was between female attractivity and estrogen levels found that the more advanced the estrous con- (Beach, 1976; Baum et al., 1977). Hausfater dition of the female, the more exclusively was (1975) suggests that in yellow baboons a sexual copulation confined to high ranking males (Hall, pheromone may be the mechanism governing 1962; DeVore and Hall, 1965). Moreover, there cycle day and individual selectivity. If so, it is are some females with whom the dominant males unlikely that a female who decreased her non- do not consort at all. For example, Hausfater hormonal estrus signs but retained her hormonal (1975) found that when three female yellow ba- estrus signs would be unattractive to dominant boons were in estrus, two different first ranking males. Since estrogen is an agent in ovulation, males did not consort with them even if no other it is necessarily present in high concentration estrous females were present in the group. during ovulation. Therefore, in the loss of estrus. Goodall (1965, 1968) found that female chim- the hormonal cues to ovulation could not have panzees during their first few sexual swellings been obscured through a reduction in appeared unattractive to mature males, but fre- production. Symons (1979) suggests that the loss 36 Beverly I. Strassmann of estrus may have begun with the continuous expense. Thus, ovulation was probably con- production of estrogen, or a pheromone based cealed through the direct dampening of its visual on estrogen. Another possibility is that there was signs and the masking of its hormonal signs. a slight alteration in an estrogen based phero- mone that, in association with the dampened visual signs, deterred high ranking males from The Diversion of Mating Effort into Paternal mating with females concealing ovulation. Se- Effort lection for males to detect the new pheromone Since the offspring of indulgent males would re- and associate it with ovulation would be espe- ceive the most paternal care, they would have cially weak if it varied among females. The vol- a competitive advantage over the offspring of atile organic constituents of the vaginal secre- more polygynous males. Compared to the pa- tions of modern humans have been shown to ternal strategy, the polygynous strategy would vary (Preti and Huggins. 1975). The visual signs become increasingly less successful. Females of ovulation may have been lost through a neo- who concealed ovulation would, on the average, tenous reduction in the sexual skin or in the have more indulgent mates and achieve greater sensitivity of the sexual skin to estrogen. reproductive success than females who adver- tised ovulation. Eventually, females with a con- spicuous estrus would no longer exist, nor would Extended Sham Estrus Versus Direct Loss of there be males exploiting this by em- Estrus phasizing mating effort over paternal effort. Fe- It is doubtful that females concealed ovulation male willingness to mate would gradually have by extending the duration of estrus signs, making extended throughout the be- sham estrus indistinguishable from true estrus, cause as long as receptivity was keyed to the as has been suggested (Alexander and Noonan, ovulatory phase ovulation would not have been 1979: Burley, 1979; Symons, 1979). This ploy concealed. would have been less likely to allow females to Polygynous behavior would not disappear, grant paternal males a high confidence of pa- but each male would mate with fewer females ternity than would the concealment of ovulation on the average and would exhibit more paternal through the direct loss or disguisement of es- care. Several factors explain why polygynous trous cues. One could expect the most success- behavior would not be lost entirely. First, ful polygynists not to copulate with females who greater access to resources that are a component extended their signs because the longer period of paternal care would enable some males to of consortship necessary to give a high proba- have more mates or seek more matings than bility of conception would reduce the number would be the case for most males. Second, there of less costly matings these males could secure. are diminishing returns from paternal care after However, females in prolonged sham estrus a certain level of indulgence. Third, although would occasionally be exposed to high ranking paternal care restricts mating effort overall, sit- males from outside their group. Hrdy (1977, uations would arise in which males could secure 1979) observed that female langurs in sham es- additional mates or copulations without invok- trus who are ignored by resident males are often ing a disadvantageous trade-off with paternal sought after by extra-troop males. She attributes care. this behavioral discrepancy to differences in the ability of resident and nonresident males to mon- itor females’ cycles, and thereby distinguish Paternal Investment: Male Versus Female pseudo-estrus from true estrus. Thus, polygyn- Advantages ous males from outside the’band would probably Burley (1979) has argued that concealed ovula- attempt copulations with hominid females in tion would not evolve to induce males into pro- sham estrus. Such males would compromise the viding paternal care because males would in- confidence of paternity of the paternal males crease their paternal investment anyway when who mated with females who concealed ovula- this behavior became advantageous for them. tion through sham estrus. Moreover, extension This assertion ignores the probable existence of of such estrous cues as sexual swellings would a stage in human evolution in which increased probably impose on females a great energetic paternal investment would have benefited fe- Concealed Ovulation in Humans 37 males greatly but would not yet have been bond with males of superior genetic fitness strongly selected for among males. In a poly- (Alexander, 1975). gynous , subordinate males would In either case, conscious knowledge of ovulation have had the most to gain by paternal behavior would be selected against because it would but their low confidence of paternity would have hinder the ability of females to deceive males restricted the development of their paternal and promote paternal care (see Alexander and tendencies. It cannot be assumed that the high Noonan, 1979; Benshoof and Thornhill, 1979). ranking males would have increased their pa- In the second case, there would be selected (or ternal investment since these males would al- never lost in the first place) subconscious phys- ready have been achieving high reproductive iological and psychological correlates of ovula- success through a reproductive strategy empha- tion that increase the probability that isolated sizing mating effort. If these males increased matings with more fit males result in pregnancy. their investment, time and energy constraints An example is facilitated sperm transport men- would then have reduced the total number of tioned by Benshoof and Thomhill (1979). matings they secured, making increased invest- ment a marginal advantage at best. It could even have been disadvantageous because it would PHYSIOLOGICAL AND PSYCHOLOGICAL probably have increased the number of matings CORRELATES OF OVULATION secured by lower ranking males or raised the confidence of paternity of lower ranking males, A review of the subject of ovulation reveals an enabling them to be more paternal. Therefore, array of physiological correlates. Concomitant a female adaptation that increased the advan- with the various hormonal changes around ovu- tages of paternal investment to males could have lation are various changes in the cervical secre- been favorably selected.-The hypothesis ad- tions that increase the ability of sperm to mi- vanced in this paper is that concealed ovulation grate. When coupled with sexual arousal in the enhanced the advantages of paternal care to sub- female, they increase the probability of concep- ordinate males by increasing their confidence of tion (Levin and Wagner, 1977). Hormonal changes paternity. Assuming that paternal care was a in the ovarian cycle of the human female have more important determinant of offspring success been shown to effect the CNS and cause changes than the dominance status of the , con- in sensory stimuli. Diamond et al. (1972) found cealed oculation would have benefited females that visual sensitivity built up to a peak at mid- and therefore been positively selected. cycle and remained high until menstruation when it dropped precipitously. Women taking nonsequential oral contraceptives, and men tested by the same procedures, did not undergo PREDICTIONS significant visual threshold changes. Laws (1977) discovered that changes in the neuroendocrine If concealed ovulation evolved because it in- system lower the acoustic reflex threshold of creased the reproductive advantages that males women using oral contraceptives or at day 16 in could gain from paternal effort relative to mating their menstrual cycle. Semesuk et al. (cited in effort, certain predictions should follow: Diamond et al., 1972) also found changes in If paternal care were sufficiently important acoustic sensitivity to be related to the menstrual in determining offspring success so that a cycle. Olfactory sensitivity of women for invo- male’s genes unrelated to paternal care were latile compounds has been correlated with the relatively trivial, then one would expect the menstrual cycle and estrogen production, with ability of females to control conception to be the greatest sensitivity occurring around ovu- relatively poorly developed and cuckoldry to lation (Le Magnen, 1950; Schneider et al., 1958; be rare. Good et al. 1976; Mair et al., 1978). Sensitivity If, however, genes irrelevant to paternal care to pain was found to decrease during ovulation were still significant in determining repro- by Buselli et al. (cited in Diamond et al., 1972). ductive success, one would expect females In addition to the physiological changes, a to retain the ability to exploit occasional low periodicity in psychological state is related to risk opportunities to mate outside the pair- the ovarian cycle. Several studies show that 38 Beverly 1. Strassmann

aggression, anxiety, inner-directed hostility, and classroom lectures. This paper has benefited greatly fatigue are lowest at mid-cycle while libido is from informative and discerning comments he offered highest (McCance et al., 1937; Benedek and on all drafts. I also appreciate the helpful suggestions Rubenstein, 1939; Altmann et al., 1941: Hart, of Gerald Borgia, Katharine Noonan, Donald Symons. 1960; Gottschalk et al., 1962; Moos, 1969: and Randy Thornhill. Nancy Burley, Lee Benshoof, and Randy Thornhill obligingly sent me their prepub- Luschen and Pierce. 1972). Other studies show lication manuscripts. Joan Strassmann provided much a premenstrual or postmenstrual rise in con- encouragement. scious sexual desire (e.g., Kinsey, 1953). The curve showing that sexual arousal peaks during ovulation found by Altmann et al. (1941) and Moos (1969) corresponded closely to a curve for REFERENCES ..______visual sensitivity (Diamond et al., 1972). Adams et al. (1978) found an increase in female initiated Adams, D.B., Gold, A.R. Burt, A.D. Rise in female sexual behavior during ovulation. initiated sexual activity at ovulation and its Tests of the physiological and psychological suppression by oral contraceptives. N~M, England Journal oJ‘Medic,ine 229(21): 1145-l 150 (1978). correlates of ovulation in nonhuman primates Alexander, R.D. The evolution of . would be helpful in determining whether these Ann. Rev. of Ecol. and Syst. 5: 325-383 (1974). traits are vestigial, or attributes that selection --. Natural selection and specialized chorusing be- has actively retained or even heightened in hu- havior in acoustical insects. In In.rects. Scietwe md mans. Of course, analysis of these correlates is Soc,iety, D. Pimentel (Ed.). Ithaca. NY: Cornell complicated since one explanation could not ac- Univ. Press, 1975. count for all of them. Beyond the idea that these -, Hoogland, J.L. Howard, R.D. Noonan. K.M. correlates are simply vestigial remnants of es- Sherman, P.W. Sexual dimorphisms and breeding trus, there are at least three possible explana- systems in pinnipeds. ungulates. primates, and hu- tions for their occurrence. The marked improve- mans. In Evolutioncrry und Human Social Behavior: An Anfhropologiccrl Perspec,tive. N.A. ment in acoustic, visual, and olfactory sensitivity Chagnon and W.G. Irons (Eds.). North Scituate, during ovulation may have improved the ability MA: Duxbury Press, 1979. of females to avoid rapists operating by stealth -, Noonan, K.M. Concealment of ovulation. pa- or ambush. In the literature on ovulation, the rental care, and human social evolution. In Eva- correlates are widely regarded as a mechanism lutionary Biology und Humon Sock/ Behavior: An to increase the probability of conception (e.g., Anthropological Perspective, N.A. Chagnon and Diamond et al., 1972). Diamond et al. assert that W.G. Irons (Eds.). North Scituate. MA: Duxbury the psychological and sensory changes could in- Press. 1979. crease the probability of coitus occurring during -, Borgia, G. On the origin and basis of the male ovulation because of the combined effect of female phenomenon. In Se.rual Selection in fnsecrs, M.F. Blum and N.A. Blum (Eds.). New York: greater sensitivity to arousing stimuli and de- Adademic Press, 1979. creased sensitivity to pain. A third possibility is Altmann, M., Knowles, E., Bull, H.D. A psychoso- that the psychological and sensory changes matic study of the sex cycle in women. Psychosom. tempt females to mate outside the pair-bond with Med. 3: 199-225 (1941). males having superior genes. This explanation Bateman, A.J. Intrasexual selection in Drosophila. supports the hypothesis that concealed ovula- Heredity 2: 349-368 (1948). tion evolved because it allowed females to pro- Baum, M.J.. Everitt, B.J. Herbert, J. Keverne, mote paternal care among the males most prone E.B. Hormonal basis of proceptivity and receptiv- to it anyway, but who were not necessarily the ity in female primates. Arc,hives of Sexuul Behavior optimal genetic of their offspring. How- 6: 173-192 (1977). Beach, F.A. Sexual attractivity, proceptivity, and re- ever, matings outside the pair-bond would not ceptivity in female . und Be- be expected to be sufticiently successful that the huvior 7: 105-138 (1976). paternal males would have a low confidence of Benedek, T., Rubenstein. B.B. The correlations be- paternity. tween ovarian activity and psychodynamic pro- cesses: I. The ovulatory phase. Psychosom. Med. I : 245-270 (1939). I thank Richard Alexander for introducing the topic of Benshoof, L., Thornhill, R. The evolution of monog- concealed ovulation in one of his many interesting amy and concealed ovulation in humans. Journal Concealed Ovulation in Humans 39

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