Strassmann 1981 Ethol Sociobiol, Evol Ovulacion Oculta

8/20/2019 Strassmann 1981 Ethol Sociobiol, Evol Ovulacion Oculta

1/10

Sexual Selection, Paternal Care, and Concealed

Ovulation in Humans

Beverly I. Strassmann

Changes in the social structure of early humans greatly

enhanced the potential for paternal care to contribute

to offspring success. Selection therefore favored females

who mated with more paternal males. Since paternal

care limits mating effort, males least successful as po-

lygynists would have the most to gain by paternal be-

havior, while the successful polygynists would gain least.

Concealed ovulation may have evolved because it pro-

moted the paternal tendencies of the less polygynous

males who advanced female reproductive success the

most. Since the offspring of indulgent males would have

a competitive advantage over the offspring of more po-

lygynous males, and females revealing the time of ovu-

lation would become increasingly scarce, all males would

eventually pursue a reproductive strategy emphasizing

paternal effort over mating effort.

In nonhuman primates the most polygynous males

mate selectively with females who are likely to be ovu-

lating. Sueh males would probably not mate with females

having dhninished cues to the time of ovulation. The

more paternally prone males could therefore consort

with these females and experience a high confidence of

paternity. Another characteristic of nonhuman primates

is that the most successful polygynists tend to have a

high dominance rank. Thus, female hominlds who mated

with more paternal males may have sacrlflced having

offspring with some of the gene advantages that con-

tribute to dominance. However, subconscious physiolog-

ical and psychological correlates of ovulation in humans

may have tempted females to exploit infrequent, low-

risk opportunities to mate outside the pair-bond with

males of superior genetic fitness. These correlates may

also promote conception irrespective of mating partner,

or they may have helped females avoid rape.

Key Words: Concealed ovulation; Dominance rank;

Estrus; Paternal care; Polygyny; Reproductive stra-

tegies; Sexual selection.

Received April 3, 1980;accepted October 16, 1980

Address

reprint requests to: Beverly I. Strassmann, c/o

Dept. of Entomology, Comstock Hall, Cornell University,

Ithaca, NY 14853.

INTRODUCTION

In the superfamily Hominoidea, human females

are unique in that they may be sexually receptive

at any time of their cycle and do not exhibit a

phase of pronounced physiological or behavioral

estrous cues that overtly signal ovulation to

themselves or to males (Butler, 1974; Alexander

and Noonan, 1979; Benshoof and Thornhill,

1979; Burley, 1979; Hrdy, 1979; Symons, 1979).

Thus, in the evolutionary line leading to humans,

there clearly has been selection to conceal ovu-

lation. Understanding the selective background

that led to the concealment of ovulation in hu-

mans could improve our understanding of inter-

actions between the sexes and provide insight

helpful in improving contraceptive methods. The

present paper will (1) review five recent hy-

potheses on the evolution of concealed ovulation

and (2) employ the theory of sexual selection to

modify the scenario proposed by Alexander and

Noonan (1979). The resulting hypothesis is sup-

ported by behaviors of primates, and it is con-

sistent with a possible explanation of the sub-

conscious physiological and psychological

correlates of human ovulation.

PREVIOUS HYPOTHESES

Burley (1979) proposes that concealed ovulation

evolved to counteract a tendency of hominid fe-

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-

ience of having children, stem from the evolution

of a large cerebrum. However, if a large cere-

brum were responsible for such dramatically

31

Ethology and Sociobiology 2: 31-40 (1981)

0 Elsevier North Holland, Inc.. 1981

52 Vanderbilt Ave., New York, New York 10017

0162-3095/81/0100031-10 02.50


2/10

32 Beverly I. Strassmann

nonadaptive behavior its disadvantages would

probably have outweighed its advantages. More-

over, studies of nonhuman primates make it

doubtful that females in obvious estrus could

have thwarted attempts by males to impregnate

them. Selection for concealed ovulation as a

means of promoting conception therefore would

not have occurred. Burley’s conclusion that

there is an apparent lack of female initiation of

copulation during ovulation is contradicted by

a study reporting an ovulatory peak in female-

initiated sex (Adams et al., 1978). Adams et al.

attribute the conflicting results of earlier studies

(e.g., McCance et al., 1937; James, 1971; Spitz

et al., 1975) to measures of sexual activity in

which the ovulatory rise in female-initiated cop-

ulations is masked by male-initiated copulations.

Hrdy (1979) suggests that concealed ovula-

tion evolved among prehominid females as a

means of confusing paternity so that males

would not be able to selectively kill the offspring

of other males. This model may explain sham

estrus in Hanuman langurs

Presbyt is ~ntelus)

but does not fit the evidence on prehominid so-

cial structure. The primates from whom humans

evolved probably experienced strong competi-

tion between groups, thus enhancing unity and

cooperation within groups. Selection for coop-

erative hunting and predator defense would also

have reinforced group solidarity (e.g., Alex-

ander, 1974). If males in a troop gained by co-

operating with each other they would not have

profited from killing each other’s offspring. As

Hrdy points out, in Savannah baboons (Papio

c~nocephnlus) the males cooperate in predator

defense and females have not evolved concealed

ovulation. According to Hrdy, “any male who

killed offspring belonging to a male still present

in the troop would reduce the stake that male

had in risking his life to defend the troop. Hence

all infants in a troop containing an infanticidal

male (including his own) would have been less

likely to survive.” Moreover, in an affiliative

troop, relatives and consorts of mothers would

help them defend their infants from attacking

males (Smuts, in preparation, cited in Hrdy,

1979). Bygott (1979) asserts that exaggerated

aggression over access to females will be pun-

ished, since selfish males will not be able to par-

ticipate in beneficial coalitions.

Hrdy claims that continuous receptivity was

part of the physiological heritage that prehom-

inid females brought to the new lifestyle, distin-

guishing humans from other primates. She may

mean that concealed ovulation evolved in a com-

mon ancestor to the Hominoidea (great apes and

humans). At such an early stage in evolution,

prehominids might not yet have become partic-

ularly cooperative within groups. This idea is

implausible since humans are the only members

of the superfamily Hominoidea who have con-

cealed ovulation.

Even if cooperation within groups is strong,

it could be argued that concealed ovulation

evolved to counteract infanticide practiced by

males from outside the group. Evidence provided

by Bygott (1979) indicates that chimpanzees

(Pan t roglod.y ty t rs) of the same troop have few

aggressive encounters over females, while in-

tergroup competition for females is fierce and

sometimes involves infanticide. Similarly, infan-

ticide among the Yanoama is often associated

with the exchange of women in intercommunity

warfare (Biocca, 1969). However, when infan-

ticide is practiced on the infants already born to

mothers recruited into a different group, males

of the new troop may be quite certain they did

not sire the infants. In this situation, the evo-

lution of concealed ovulation would only benefit

females who switched groups early in pregnancy

before their condition could be detected by

males. It is, therefore, not surprising that con-

cealed ovulation has not evolved in chimpan-

zees. These arguments imply that concealed

ovulation evolved in humans for a reason other

than intergroup infanticide. Such infanticide

would, however, increase the importance of pa-

ternal care; this could have been a precipitating

factor in the evolution of concealed ovulation

(Alexander and Noonan, 1979).

Symons (1979) offers two scenarios to explain

the loss of estrus in humans. In one, humans

live in promiscuous polygynous bands and males

give meat to females in exchange for sex. Ac-

cording to Symons, this practice caused females

to prolong their stage of sexual attractiveness.

However, males who mated only with females

in true estrus would have been selected for rel-

ative to males who mated with females in either

true or sham estrus. Unless one assumes that

such discriminating males were extremely scarce.

it is questionable whether females who pro-

longed estrus would have been given more meat

and thus been favored by selection.

In another scenario, Symons (1979) and Ben-

shoof and Thornhill (1979) suggest that con-


3/10

Concealed Ovulation in Humans

33

cealed ovulation evolved to facilitate cuckoldry.

The authors assert that females who did not ad-

vertise ovulation would have minimized the ca-

pacity of their mates to monitor their reproduc-

tive cycles and guard them during ovulation. If

at the time concealed ovulation evolved the

human breeding system was monogamous or

harem polygynous (and females sometimes had

access to males who were genetically superior

to their mates), the cuckoldry scenario is cred-

ible. However, it is doubtful that females would

evolve induced ovulation or another trait that

would perfect their ability to cuckold males.

Otherwise their mates would have such low con-

fidence of paternity that selection would dim-

inish their paternal care-whether or not males

discovered infidelities.

Alexander and Noonan’s hypothesis regard-

ing the evolution of concealed ovulation is based

on the following assumptions: (1) At the time

ovulation became concealed human society was

polygynous and consisted of multimale bands.

Several studies link early humans with this social

system (Lee and DeVore, 1968; Jolly, 1972;

Alexander et al., 1979; Brace, 1979; Campbell,

1979). (2) During this period in human evolution

paternal care became an increasingly important

determinant of offspring success. The increasing

importance of paternal care, according to Alex-

ander and Noonan, is associated with intergroup

competition and the growth in group size and

unity. These developments increased the com-

plexity of social interactions and aggravated ju-

venile disadvantages in experience and strength.

Therefore, parents who conveyed to their off-

spring the knowledge and skills needed for making

the best decisions in complex social situations

outreproduced less instructive parents. Other

authors point out that conflicting selection for

bipedality, which favors a narrow pelvis, and

larger brain size, which favors a wide pelvis,

could result in more altricial young whose brains

would grow large after birth (e.g., Fox, 1972:

Benshoof and Thornhill, 1979). The advantages

of a longer learning period could also promote

altriciality (Washburn’ and Lancaster, 1967:

Pfeiffer, 1972). The increasing altriciality of

human young would further enhance the advan-

tages of parternal care.

Alexander and Noonan’s two initial assump-

tions, as well as their important idea that con-

cealed ovulation evolved in the context of fe-

males securing paternal care, are an integral part

of the hypothesis advanced in this paper. Yet

the evolutionary steps they propose are differ-

ent. They suggest that through concealing ovu-

lation females forced desirable males into con-

sort relationships long enough to decrease the

males’ chances of success in securing other mat-

ings. The confidence of paternity of these males,

according to Alexander and Noonan, was si-

multaneously increased because potential com-

petitors no longer knew when females were

ovulating.

Their hypothesis implies that the highest

quality females would be in demand by the high-

est quality males and would enter into prolonged

consortships with these males before subordi-

nate females and males would enter into con-

sortships.’ It seems more likely that males most

successful as polygynists wotdd be the last to

increase their paternal care, not the first.

In order for high ranking males to abandon

their successful polygynous strategy and in-

crease their paternal investment, differentials in

female quality would have to be remarkably

steep. The relevant sample sizes are small, but

some studies of nonhuman primates seem to find

instances in which females differ markedly in

their attractiveness (Hausfater, 1975) or in their

reproductive success (Goodall, 1971), while oth-

ers point toward more uniform female quality

(e.g., Loy, 1971; Kaufmann, 1965). Further

studies are needed to determine whether steep

differentials are likely to have existed among

human females. In the absence of steep differ-

entials, high ranking males who copulated around

the most likely time of ovulation with females

having a precise estrus would probably have the

highest reproductive success.

In addition to reducing the number of estrous

females with whom a male can mate, partici-

pation in a consortship potentially has other dis-

’ “The highest quality females fin terms of ability to bear

and rear offspring, and, perhaps, to enhance their status or

other correlates of reproductive success), would be in demand

by the highest quality males most prone to polygyny; such

females could afford to prolong estrus longer than others with-

out risk of desertion by the male. Low quality females would

be at least partially excluded from mating with the highest

quality males by this ploy. Competition for matings by lower

quality males would be reduced (because top quality males

are already committed), making concealment of ovulation ad-

vantageous to low ranking females in securing at least some

parental care for their offspring” (Alexander and Noonan.

1979, p. 448).


4/10

34

Beverly I. Strassmann

advantages discussed by Hausfater (1975). He

postulates such negative consequences as re-

duced food intake resulting from the need for

constant guarding of the female, and increased

exposure to aggression and harassment from

other males. In his study of yellow baboons

(Pupio cynocephalus), the first ranking adult

males mated and consorted primarily on the op-

timal day for mating. Lower ranking adults con-

sorted on as many potentially fertile cycle days

as possible. According to Hausfater, the strategy

of the first ranking males gives them a relatively

high probability of impregnating females while

minimizing the negative consequences of con-

sortship.

High ranking males who entered into con-

sortships with females who prolonged estrus

would suffer the additional disadvantage of the

higher cost of high confidence of paternity.

When males need to guard their mate only during

the brief period of estrus, confidence of paternity

is least expensive (Benshoof and Thornhill,

1979; Burley, 1979; Symons, 1979). If a male

guards a female continuously, he compromises

his ability to hunt and carry out the other activ-

ities that are at least indirectly an important com-

ponent of paternal care. Although concealed

ovulation would greatly reduce the probability

of matings outside the pair-bond resulting in

pregnancy, the following males would still at-

tempt such matings: unmated males, males with

pregnant mates, and other males as low cost

opportunities arose. Since confidence of patern-

ity would be more expensive for high-ranking

males, it is unclear how concealed ovulation in

Alexander and Noonan’s scheme could increase

paternal investment. In view of the disadvan-

tages of consortships to dominant males, it is

necessary to add to Alexander and Noonan’s

scenario the condition that the first males to pro-

long their consortships would probably be those

having a low probability of securing matings.

Moreover, the females with whom such males

consorted would have to be sufficiently unat-

tractive to the polygynous males that their con-

sorts would have a high confidence of paternity.

CONCEALED OVULATION AND MATE

SELECTION

Due to anisogamy, which may be the ultimate

source of differential parental investment be-

tween the sexes, females are usually a limiting

resource to males (Bateman, 1948; Trivers,

1972). One consequence is a general tendency

toward polygynous breeding systems in which

there is great variance in reproductive success

among males. In their competition to secure suc-

cessful matings with females, conspecific males

have evolved alternative strategies involving

both behavioral and morphological differences.

For a recent review of alternative male strategies

among several classes of organisms see Cade

(1979).

This theoretical framework suggests a pos-

sible selective background for the evolution of

concealed ovulation. If humans were polygyn-

ous at the time concealed ovulation evolved,

some males by definition would have had more

success at securing matings resulting in preg-

nancy. Studies of nonhuman primates indicate

that those males who secure the most matings

around ovulation tend to be dominant while sub-

ordinate males find seeking matings a costly en-

deavor with a lower probability of success (see

Conaway and Koford, 1965; DeVore, 1965:

Kaufmann, 1965; Lindburg, 1971; Loy, 1971:

Hausfater, 1975). Those males who are least suc-

cessful as polygynists would tend to expend

greater paternal effort on the offspring that they

produced with a relatively limited number of fe-

males. In fact, their options for increasing their

reproductive success would resemble those of

females. The successful polygynists, on the con-

trary, would tend to expend less paternal effort

on each of the offspring of a larger number of

females. This argument is based on the assump-

tion that time and energy spent on mating effort

will limit paternal effort (see Alexander and Bor-

gia, 1979). Borgia (1979) formulates the similar

argument that males who are unlikely to be suc-

cessful at securing matings because of their rel-

atively low genetic fitness may enhance their

reproductive success by providing females and

their young with material benefits. Of course,

greater paternal effort on the part of subordinate

males would have to be associated with en-

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-

terminant of offspring success increased so as

to exceed the importance of the male’s genetic

assets which do not contribute to paternal care,

those males least able to monopolize matings


5/10


35

would have become the most desirable mates.

These arguments suggest that concealed ovula-

tion evolved because it favored the strategy of

the subordinate, more paternal males who pro-

moted female reproductive success the most.

Females sacrificed the genetic benefits offered

by the high ranking males in exchange for the

more important paternal benefits offered by

lower ranking males. Borgia (1979) also arrives

at the conclusion that females sometimes must

compromise potential gain from either the ma-

terial or the genetic benefits offered by males in

order to maximize reproductive success.

How would the concealment of ovulation en-

hance the confidence of paternity of the subor-

dinate males? Subordinate males could probably

keep their consorts from copulating with other

low ranking males, but not from the high ranking

males. However, if females who concealed ovu-

lation were sufficiently unattractive to the high

ranking males, their lower ranking consorts

would have a higher confidence of paternity.

Female Attractivity

Behaviors of nonhuman primates indicate that

females who concealed ovulation by gradually

dampening their estrus signs might have been

unattractive to the dominant males. Observa-

tions of baboons, rhesus monkeys, and chim-

panzees reveal a strong degree of selectivity in

the mating of the dominant males. First ranking

male yellow baboons do not mate on all the po-

tentially fertile days of a female’s cycle, but in-

stead constrain their mating to the optimal day,

sometimes even the optimal time of day (Haus-

fater, 1975). On the optimal day estrus signs such

as sexual swellings are most pronounced. In

other studies of baboons (Papio w-sinus and P.

am is)

and macaques

(Macaca mulatta),

it was

found that the more advanced the estrous con-

dition of the female, the more exclusively was

copulation confined to high ranking males (Hall,

1962; DeVore and Hall, 1965). Moreover, there

are some females with whom the dominant males

do not consort at all. For example, Hausfater

(1975) found that when three female yellow ba-

boons were in estrus, two different first ranking

males did not consort with them even if no other

estrous females were present in the group.

Goodall (1965, 1968) found that female chim-

panzees during their first few sexual swellings

appeared unattractive to mature males, but fre-

quently solicited mounting from adolescents.

Since dominant males cue in on estrus signs and

do not mate with females with partial swellings,

they might pass up opportunities to mate with

females who had begun to reduce their estrus

signs, even though these females would be fer-

tile. This behavior would reflect an inability of

the males to distinguish between females un-

likely to be fertile and females concealing ovu-

lation. Low ranking males would probably mate

with females who dampened their estrus signs

because they mate with females having partial

swellings.

It is probable that at the time concealed ovu-

lation evolved all males including the dominant

ones already wqre somewhat inclined to be pa-

ternal-perhaps bnly through protecting past or

present female c sorts or their young. Such

behavior is thought TO occur to some extent in

all the great apes (Mitchell, 1969) and would re-

duce the time and energy available to the dom-

inant males to seek suboptimal matings. Domi-

nant males would be especially disinclined to

attempt copulations with females appearing su-

boptimal if these females were being vigorously

defended by their low ranking male consorts.

Since their matings with females appearing su-

boptimal would be rare, dominant males would

not experience strong selection for the ability to

distinguish between females concealing ovula-

tion and females unlikely to be fertile. The rare

matings that would occur between dominant

males and females concealing ovulation would

not diminish the paternal behavior of the fe-

males’ indulgent consorts because the latter

would have been copulating with the females

much more regularly and therefore would be

more likely to sire offspring.

In nonhumans there is a close correlation

between female attractivity and estrogen levels

(Beach, 1976; Baum et al., 1977). Hausfater

(1975) suggests that in yellow baboons a sexual

pheromone may be the mechanism governing

cycle day and individual selectivity. If so, it is

unlikely that a female who decreased her non-

hormonal estrus signs but retained her hormonal

estrus signs would be unattractive to dominant

males. Since estrogen is an agent in ovulation,

it is necessarily present in high concentration

during ovulation. Therefore, in the loss of estrus.

the hormonal cues to ovulation could not have

been obscured through a reduction in hormone

production. Symons (1979) suggests that the loss


6/10

36 Beverly I. Strassmann

of estrus may have begun with the continuous

production of estrogen, or a pheromone based

on estrogen. Another possibility is that there was

a slight alteration in an estrogen based phero-

mone that, in association with the dampened

visual signs, deterred high ranking males from

mating with females concealing ovulation. Se-

lection for males to detect the new pheromone

and associate it with ovulation would be espe-

cially weak if it varied among females. The vol-

atile organic constituents of the vaginal secre-

tions of modern humans have been shown to

vary (Preti and Huggins. 1975). The visual signs

of ovulation may have been lost through a neo-

tenous reduction in the sexual skin or in the

sensitivity of the sexual skin to estrogen.

Extended Sham Estrus Versus Direct Loss of

Estrus

It is doubtful that females concealed ovulation

by extending the duration of estrus signs, making

sham estrus indistinguishable from true estrus,

as has been suggested (Alexander and Noonan,

1979: Burley, 1979; Symons, 1979). This ploy

would have been less likely to allow females to

grant paternal males a high confidence of pa-

ternity than would the concealment of ovulation

through the direct loss or disguisement of es-

trous cues. One could expect the most success-

ful polygynists not to copulate with females who

extended their signs because the longer period

of consortship necessary to give a high proba-

bility of conception would reduce the number

of less costly matings these males could secure.

However, females in prolonged sham estrus

would occasionally be exposed to high ranking

males from outside their group. Hrdy (1977,

1979) observed that female langurs in sham es-

trus who are ignored by resident males are often

sought after by extra-troop males. She attributes

this behavioral discrepancy to differences in the

ability of resident and nonresident males to mon-

itor females’ cycles, and thereby distinguish

pseudo-estrus from true estrus. Thus, polygyn-

ous males from outside the’band would probably

attempt copulations with hominid females in

sham estrus. Such males would compromise the

confidence of paternity of the paternal males

who mated with females who concealed ovula-

tion through sham estrus. Moreover, extension

of such estrous cues as sexual swellings would

probably impose on females a great energetic

expense. Thus, ovulation was probably con-

cealed through the direct dampening of its visual

signs and the masking of its hormonal signs.

The Diversion of Mating Effort into Paternal

Effort

Since the offspring of indulgent males would re-

ceive the most paternal care, they would have

a competitive advantage over the offspring of

more polygynous males. Compared to the pa-

ternal strategy, the polygynous strategy would

become increasingly less successful. Females

who concealed ovulation would, on the average,

have more indulgent mates and achieve greater

reproductive success than females who adver-

tised ovulation. Eventually, females with a con-

spicuous estrus would no longer exist, nor would

there be males exploiting this physiology by em-

phasizing mating effort over paternal effort. Fe-

male willingness to mate would gradually have

extended throughout the menstrual cycle be-

cause as long as receptivity was keyed to the

ovulatory phase ovulation would not have been

concealed.

Polygynous behavior would not disappear,

but each male would mate with fewer females

on the average and would exhibit more paternal

care. Several factors explain why polygynous

behavior would not be lost entirely. First,

greater access to resources that are a component

of paternal care would enable some males to

have more mates or seek more matings than

would be the case for most males. Second, there

are diminishing returns from paternal care after

a certain level of indulgence. Third, although

paternal care restricts mating effort overall, sit-

uations would arise in which males could secure

additional mates or copulations without invok-

ing a disadvantageous trade-off with paternal

care.

Paternal Investment: Male Versus Female

Advantages

Burley (1979) has argued that concealed ovula-

tion would not evolve to induce males into pro-

viding paternal care because males would in-

crease their paternal investment anyway when

this behavior became advantageous for them.

This assertion ignores the probable existence of

a stage in human evolution in which increased

paternal investment would have benefited fe-


7/10


7

males greatly but would not yet have been

strongly selected for among males. In a poly-

gynous primate species, subordinate males would

have had the most to gain by paternal behavior

but their low confidence of paternity would have

restricted the development of their paternal

tendencies. It cannot be assumed that the high

ranking males would have increased their pa-

ternal investment since these males would al-

ready have been achieving high reproductive

success through a reproductive strategy empha-

sizing mating effort. If these males increased

their investment, time and energy constraints

would then have reduced the total number of

matings they secured, making increased invest-

ment a marginal advantage at best. It could even

have been disadvantageous because it would

probably have increased the number of matings

secured by lower ranking males or raised the

confidence of paternity of lower ranking males,

enabling them to be more paternal. Therefore,

a female adaptation that increased the advan-

tages of paternal investment to males could have

been favorably selected.-The hypothesis ad-

vanced in this paper is that concealed ovulation

enhanced the advantages of paternal care to sub-

ordinate males by increasing their confidence of

paternity. Assuming that paternal care was a

more important determinant of offspring success

than the dominance status of the father, con-

cealed oculation would have benefited females

and therefore been positively selected.

PREDICTIONS

If concealed ovulation evolved because it in-

creased the reproductive advantages that males

could gain from paternal effort relative to mating

effort, certain predictions should follow:

If paternal care were sufficiently important

in determining offspring success so that a

male’s genes unrelated to paternal care were

relatively trivial, then one would expect the

ability of females to control conception to be

relatively poorly developed and cuckoldry to

be rare.

If, however, genes irrelevant to paternal care

were still significant in determining repro-

ductive success, one would expect females

to retain the ability to exploit occasional

ow

risk opportunities to mate outside the pair-

bond with males of superior genetic fitness

(Alexander, 1975).

In either case, conscious knowledge of ovulation

would be selected against because it would

hinder the ability of females to deceive males

and promote paternal care (see Alexander and

Noonan, 1979; Benshoof and Thornhill, 1979).

In the second case, there would be selected (or

never lost in the first place) subconscious phys-

iological and psychological correlates of ovula-

tion that increase the probability that isolated

matings with more fit males result in pregnancy.

An example is facilitated sperm transport men-

tioned by Benshoof and Thomhill (1979).

PHYSIOLOGICAL AND PSYCHOLOGICAL

CORRELATES OF OVULATION

A review of the subject of ovulation reveals an

array of physiological correlates. Concomitant

with the various hormonal changes around ovu-

lation are various changes in the cervical secre-

tions that increase the ability of sperm to mi-

grate. When coupled with sexual arousal in the

female, they increase the probability of concep-

tion (Levin and Wagner, 1977). Hormonal changes

in the ovarian cycle of the human female have

been shown to effect the CNS and cause changes

in sensory stimuli. Diamond et al. (1972) found

that visual sensitivity built up to a peak at mid-

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

significant visual threshold changes. Laws (1977)

discovered that changes in the neuroendocrine

system lower the acoustic reflex threshold of

women using oral contraceptives or at day 16 in

their menstrual cycle. Semesuk et al. (cited in

Diamond et al., 1972) also found changes in

acoustic sensitivity to be related to the menstrual

cycle. Olfactory sensitivity of women for invo-

latile compounds has been correlated with the

menstrual cycle and estrogen production, with

the greatest sensitivity occurring around ovu-

lation (Le Magnen, 1950; Schneider et al., 1958;

Good et al. 1976; Mair et al., 1978). Sensitivity

to pain was found to decrease during ovulation

by Buselli et al. (cited in Diamond et al., 1972).

In addition to the physiological changes, a

periodicity in psychological state is related to

the ovarian cycle. Several studies show that


8/10

8

Beverly 1. Strassmann

aggression, anxiety, inner-directed hostility, and

fatigue are lowest at mid-cycle while libido is

highest (McCance et al., 1937; Benedek and

Rubenstein, 1939; Altmann et al., 1941: Hart,

1960; Gottschalk et al., 1962; Moos, 1969:

Luschen and Pierce. 1972). Other studies show

a premenstrual or postmenstrual rise in con-

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

urve

for

visual sensitivity (Diamond et al., 1972). Adams

et al. (1978) found an increase in female initiated

sexual behavior during ovulation.

Tests of the physiological and psychological

correlates of ovulation in nonhuman primates

would be helpful in determining whether these

traits are vestigial, or attributes that selection

has actively retained or even heightened in hu-

mans. Of

course, analysis of these correlates is

complicated

since one explanation could not ac-

count for all of them. Beyond the idea that these

correlates are simply vestigial remnants of es-

trus, there are at least three possible explana-

tions for their occurrence. The marked improve-

ment in acoustic, visual, and olfactory sensitivity

during ovulation may have improved the ability

of females to avoid rapists operating by stealth

or ambush. In the literature on ovulation, the

correlates are widely regarded as a mechanism

to increase the probability of conception (e.g.,

Diamond et al., 1972). Diamond et al. assert that

the psychological and sensory changes could in-

crease the probability of coitus occurring during

ovulation because of the combined effect of

greater sensitivity to arousing stimuli and de-

creased sensitivity to pain. A third possibility is

that the psychological and sensory changes

tempt females to mate outside the pair-bond with

males having superior genes. This explanation

supports the hypothesis that concealed ovula-

tion evolved because it allowed females to pro-

mote paternal care among the males most prone

to it anyway, but who were not necessarily the

optimal genetic fathers of their offspring. How-

ever, matings outside the pair-bond would not

be expected to be sufticiently successful that the

paternal males would have a low confidence of

paternity.

I thank Richard Alexander for introducing the topic of

concealed ovulation in one of his many interesting

classroom lectures. This paper has benefited greatly

from informative and discerning comments he offered

on all drafts. I also appreciate the helpful suggestions

of Gerald Borgia, Katharine Noonan, Donald Symons.

and Randy Thornhill.

Nancy

Burley, Lee Benshoof,

and Randy Thornhill obligingly sent me their prepub-

lication manuscripts. Joan Strassmann provided much

encouragement.

REFERENCES

..______

Adams, D.B., Gold, A.R. Burt, A.D. Rise in female

initiated sexual activity at ovulation and its

suppression by oral contraceptives. N~M, England

Journal

oJ‘Medic,ine 229(21): 1145-l 150 (1978).

Alexander, R.D. The evolution of social behavior.

Ann. Rev. of Ecol. and Syst. 5: 325-383 (1974).

--. Natural selection and specialized chorusing be-

havior in acoustical insects. In In.rects.

Scietwe md

Soc,iety,

D. Pimentel (Ed.). Ithaca. NY: Cornell

Univ. Press, 1975.

-, Hoogland, J.L. Howard, R.D. Noonan. K.M.

Sherman, P.W. Sexual dimorphisms and breeding

systems in pinnipeds. ungulates. primates, and hu-

mans. In Evolutioncrry Biology und Human Social

Behavior: An Anfhropologiccrl Perspec,tive. N.A.

Chagnon and W.G. Irons (Eds.). North Scituate,

MA: Duxbury Press, 1979.

-, Noonan, K.M. Concealment of ovulation. pa-

rental care, and human social evolution. In Eva-

lutionary Biology und Humon Sock/ Behavior: An

Anthropological Perspective,

N.A. Chagnon and

W.G. Irons (Eds.). North Scituate. MA: Duxbury

Press. 1979.

-, Borgia, G. On the origin and basis of the male

female phenomenon. In Se.rual

Selection in fnsecrs,

M.F. Blum and N.A. Blum (Eds.). New York:

Adademic Press, 1979.

Altmann, M., Knowles, E., Bull, H.D. A psychoso-

matic study of the sex cycle in women. Psychosom.

Med. 3: 199-225 (1941).

Bateman, A.J. Intrasexual

selection in Drosophila.

Heredity 2: 349-368 (1948).

Baum, M.J.. Everitt, B.J. Herbert, J. Keverne,

E.B. Hormonal basis of proceptivity and receptiv-

ity in female primates.

Arc,hives of Sexuul Behavior

6: 173-192 (1977).

Beach, F.A. Sexual attractivity, proceptivity, and re-

ceptivity in female mammals.

Hormones und Be-

huvior 7: 105-138 (1976).

Benedek, T., Rubenstein. B.B. The correlations be-

tween ovarian activity and psychodynamic pro-

cesses: I.

The ovulatory phase.

Psychosom. Med.

I :

245-270 (1939).

Benshoof, L., Thornhill, R. The evolution of monog-

amy and concealed ovulation in humans. Journal


9/10

Concealed Ovulation in Humans 39

of Social and Bi ol ogical St ructur es 2: 95-106

1979).

Biocca, E. Yanoama. New York: E.P. Dutton Co.,

1969.

Borgia, G. Sexual selection and the evolution of mat-

ing systems. In

Sexual Sel ecti on and Reproducti ve

Competi ti on in nsects, M.S. Blum and N.A. Blum

(Eds.). New York: Academic Press, 1979.

Brace, C.L. Biological parameters and Pleistocene

hominid lifeways. In

Primate Ecology and Human

Or igi ns: Ecologi cal Inj luences on Social Organi-

zation, I.S. Bernstein and E.O. Smith (Eds.). New

York: Garland STPM Press, 1979.

Burley, N. The evolution of concealed ovulation.

Ameri can Na t ural ist 114 6): 835-858 1979).

Butler, H. Evolutionary trends in primate sex cycles.

Contri buti ons to Primat ology 3: 2-35 1974).

Bygott, J.D. Agonistic behavior,‘dominance, and so-

cial structure in wild chimpanzees of the Gombe

National Park. In The Great Apes, B. Hamburg and

E. McCown (Eds.). Menlo Park, CA: Benjamin/

Cummings, 1979.

Cade, W. The evolution of alternative male reproduc-

tive strategies in field crickets. In Sexual Selection

and Reproductiv e Competi ti on in Insects, M.S.

Blum and N.A. Bium (Eds.). New York: Academic

Press, 1979.

Campbell, B. Ecological factors and social organiza-

tion in human evolution. In Primate Ecology and

Human Or igins: Ecologi cal Inf luences on Social

Organization,

I.S. Bernstein and E.O. Smith (Eds.).

New York: Garland STPM Press, 1979.

Conaway, C.H., Koford, C.B. Estrous cycles and

mating behavior in a free-ranging band of rhesus

monkeys. Journal of Mammal ogy 45: 577-588

1965).

DeVore, I. Male dominance and mating behavior in

baboons. In Sex and Behavior, F.A. Beach (Ed.).

New York: Wiley, 1965.

-, Hall, K.R.L. Baboon social behavior. In Pri -

mat e Behavi or: Field St udi es

o f

Monkeys and

Apes, I. DeVore (Ed.). New York: Holt, Rinehart,

and Winston, 1965.

Diamond M., Diamond, A.L., Mast, M. Visual sen-

sitivity and sexual arousal levels during the men-

strual cycle.

Journal

o f

Nervous and M ental

Dis-

ease 155(3): 170-176 (1972).

Fox, R. Alliance and constraint: sexual selection and

the evolution of human kinship systems. In Sexual

Sel ecti on and t he Descent o f Man: 1871-1971, B.

Campbell (Ed.). Chicago: Aldine, 1972.

Good, P.R., Geary, N., Engen, T. The effect of es-

trogen on odor detection.

Chemical Senses and

Flav or 2: 45-50 1976).

Goodall, J. Chimpanzees of the Gombe Stream Re-

serve. In

Pri mat e Behavi or: Field St udi es

o f

Mon-

keys and Apes, I. DeVore (Ed.). New York: Holt,

Rinehart, and Winston, 1965.

-. The behaviour of free-living chimpanzees in the

Gombe Stream Reserve. Ani m. Behav. M onogr. 1

Part 3: 161-311 (1968).

-. In The Shadow o f Man. Boston: Houghton Mif-

flin, 1971.

Gottschalk, L.A., Kaplan, S.M. Gleser, G.C. Winget,

C.M. Variations in magnitude of emotion: A method

applied to anxiety and hostility during phases of the

menstrual cycle.

Psychosom. M ed. 24: 300-311

1962).

Hall, K.R.L. The sexual, agonistic and derived social

behaviour patterns of the wild chacma baboon,

Papi o ursinus. Pr oc. 2001. Society London 139 1 ):

238-327 1962).

Hart, R.D. Monthly rhythm of libido in married

women. Bri t ish M edi cal Journal 1: 1023-1024

1960).

Hausfater, G. Dominance and reproduction in ba-

boons Papio cynocephalus). Contri b. to Prima-

tology 7. Basel: S. Karger, 1975.

Hrdy, S. The Langurs of Abu: Femal e and M al e St ra-

tegies o f Reproduction. Cambridge, MA: Harvard

Univ. Press, 1977.

-. Infanticide among animals.

Ethology and Socio-

biology l(1): 13-40 (1979).

James, W.H. The distribution of coitus within the

human intermenstruam. J. Biosoc. Sci. 3: 159-171

(1971).

Jolly, A. The Evolution o f Primate Behavior . N ew

York: Macmillan, Co., 1972.

Kaufmann, J.H. A three-year study of mating behav-

ior in a free-ranging band of rhesus monkeys.

Ecol-

ogy 46 4): 500-512 1965).

Kinsey, A.C., and the Staff of the Institute for Sex

Research. Sexual Behavi or in t he Human Femal e.

Philadelphia: W.B. Saunders, 1953.

Laws, D.W. The effects of the normal menstrual cycle

and the use of oral contraceptives on the acoustic

reflex threshold. Di sser. Abst . I nt er. 37 7-B): 3338

1977).

Lee, R.B., DeVore, I. (Eds.). Man the Hunter. Chi-

cago: Aldine, 1968.

Le Magnen, J. Nouvelles don&es sur le phtnomene

de I’exaltolide. Comp tes Rendus de I ’A cademie des

Sciences. Paris, 1950.

Levin, R.J., Wagner, G. Human vaginal fluid ionic

composition and modification by sexual arousal.

Journal o f Physi ol ogy 266 l ): 62P-63P 1977).

Lindburg, D.G. The rhesus monkey in north India: An

ecological and behavioral study. In

Primate Be-

havior, L.A. Rosenblum (Ed.). New York: Aca-

demic Press, 1971, Vol. 2.

Loy, J. Estrous behavior of free-ranging rhesus mon-

keys

M ucaca mulat ta). Primat es 12 l ): l-31 1971).

Luschen, M.E., Pierce, D.M. Effect of the menstrual

cycle on mood and sexual arousability.

J. Sex Res.

8: 41-47 (1972).

Mair, R.G., Bouffard, J.A. Engen, T. Morton,


10/10

Beverly 1. Strassmann

T.H. Olfactory sensitivity during the menstrual

cycle. Sensory Processes 2(2): 90-98 (1978).

McCance, R.A., Luff, M.C. Widdowson, E.E. Physical

and emotional periodicity in women. J. Hyg.

(Can .)

37: 571-611 (1937).

Mitchell, G.D. Paternalistic behavior in primates. Psy-

cho/. Bulletin 71(6): 399-417 (1969).

Moos. R.H., Kopell, B.S. Melges, R.R. Yalom, I.D.

Lunde,

D.T. Clayton,

R.B. Hamburg,

D.A. Fluctuations in symptoms and moods during

the menstrual cycle. J. Psychosom. Res. 13: 37-44

(1969).

Pfeiffer, J.E. The Emergence of Man. New York:

Harper and Row, 1972.

Preti, G., Huggins, G.R. 1975. Cyclical changes ir

volatile acidic metabolites of human vaginal secre-

tions and their relation to ovulation. J. Chem. Ecol.

361-376 (1975).

Schneider, R., Costiloe, P. Howard, R. Wolf,

S. Olfactory perception thresholds in hypogonadal

women: Changes accompanying the administration

of androgen and estrogen. Journal of Clinical En-

docrinology and Metabolism 18: 379-390 (1958).

Spitz, C.J., Gold, A.R. Adams, D.B. Cognitive and

hormonal factors affecting coital frequency. Arch.

Sex. Eehav. 4: 249-263 (1975).

Symons, D.

The Evolurion of Human Sexuality. New

York: Oxford Univ. Press, 1979.

Trivers, R.L. Parental investment and sexual selec-

tion. In Sexual Selection and the Descent of Man

1871-1971, B. Campbell (Ed.). Chicago: Aldine,

1972.

Washburn, S.L., Lancaster, C.S. The evolution of

hunting. In Human Evolution: Readings in Physical

Anthropology, N. Kom and F.W. Thompson (Eds.).

New York: Holt, Rinehart and Winston, 1967.

Strassmann 1981 Ethol Sociobiol, Evol Ovulacion Oculta

Documents

Transcript of Strassmann 1981 Ethol Sociobiol, Evol Ovulacion Oculta