Loss of Estrus in Human Evolution:
Too Many Answers, Too Few
Questions
Horst D. Steklis and Catherine H. Whiteman
Department of Anthropology, Rutgers-The State University of
New Jersey
Models addressing the importance of “loss of es&us” in human evolution assume that,
as part of a general trend among higher primates, endogenous hormonal fluctuations
have less influence on human female sexuality than cognitive and socioenvironmental
factors. The diversity of reproductive patterns among primate species is not satisfac-
torily explained as the outcome of evolutionary trends along dimensions such as brain
enlargement, behavioral flexibility, or relative independence of behavior from pbysi-
ology. Rather, the role of hormones and other factors must be viewed in the context
of species’ life history and ecological constraints. Human studies on the relationship
between the menstrual cycle and sexual behavior have been limited to Western women
in industrialized societies, which may not reveal evolved behavioral-physiological pat-
terns. Furthermore, available studies have yielded inconsistent results. No single pat-
tern emerges that can be said to characterize the human female, and no conclusion can
be reached regarding the relationship between cyclic hormonal fluctuations and sexual
behavior and, thus, whether human ovulation is concealed. Future studies are needed
that are methodologically improved and systematically document the interaction among
ecological, subsistence, social, and physiological variables.
KEY WORDS: Loss of estruc: Concealed ovulation: Primate sexuality: Menstrual
cycle: Evolutionary models: Hormones and behavior.
I. INTRODUCTION zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
odels of the evolution of human sexual behavior often point
M
male-female
to the loss of estrus in women as one of the most important
events in human evolution.
of estrus is a consequence
pair bonding and cooperative
It has been proposed that the loss
of the following: 1) facilitation
male hunting (Campbell
Morris 1967; Pfeiffer 1969): 2) females trading sex for meat hunted by males,
of
1974;
which in turn led to the development of pair-bonds and increased paternal
certainty (Alexander and Noonan 197X: Fisher 1982; Hill 1982: Lovejoy
Received July IS, 1988: revised March 23. 1989
Address reprint requests to: Horst D. Steklis. Ph.D.. Department of Anthropology. Rutgers-
The State University of New Jersey. Douglass Campus. New Brunswick, NJ 08903.
Ethology and Sociobiology IO: 4 17-434 ( 1989)
r<j Elsevler Science Publishing Co.. Inc.. IYXY
6.55 Avenue of the America\. New York. NY 10010
,418 H. D. Steklis and C. H. Whiteman
1981; Symons 1979: Zcveloff and Boyce 1982): 3) female opportunistic mat-
ing with a variety of males, thereby confusing paternity, increasing male-
female alliances, and reducing infanticide (Andelman 1987: Benshoof and
Thornhill 1979; Hrdy 1979; Tanner 1981): 4) avoidance ofconception because
of the risks, pain, and workload of pregnancy, childbirth. and infant care
(Burley 1979); 5) various structural/functional changes related to bipedalism
(Manson 1986; Spuhler 1978).
Many of these proposals have assumed that the human female is unique
among primates in exhibiting continuous sexual receptivity and no overt
clues to ovulation (e.g.. Benshoof and Thornhill 1979: Fisher 1982: Strass-
mann. 1981: Zeveloff and Boyce 1982); however. examination of sexual bc-
havior in comparative perspective has led primatologists to question the
uniqueness of human female sexuality (e.g., Gray and Wolfe 19X3: Hrdy
1979: 1986: Small 1988). For example, in discussing concealed ovulation,
Andelman (1987) observed that “. . concealed ovulation is so rare that it
is often incorrectly assumed to be restricted to human females, although it
also occurs among several other species within the order Primates” (p. 785).
Similarly, a review of patterns of primate sexuality led Hrdy and Whitten
(1986) to conclude that the traditional dichotomy between humans and other
primates in the display of sexual receptivity outside the time of ovulation
‘/
. . is an oversimplification. On the one hand, human females are clearly
not receptive all the time; . . On the other hand, the information . shows
many nonhuman primate females exhibit sexual receptivity outside the brief
period right around ovulation” (p. 384).
Nonetheless, concealed ovulation and continuous sexual receptivity t-e-
main key aspects of recent models of human evolution (Ember and Embet
19X4; Shaw and Darling 1984; Tooby and DeVore 1987; Turke 1984). The
problem with these models is that despite the use of a comparative per-
spective, they nevertheless inappropriately characterize human female scx-
ual patterns. For example, Manson (1986) argues for “the presence of a
bimodal pattern of elevated sexual arousability, with peaks in the premen-
strual phase and around ovulation at midcycle” (p. 21). As we will show,
this pattern of sexual activity is not necessarily a species-typical one. Morc-
over, presently available evidence does not permit the abstraction of any
single pattern of female sexuality. We propose that current theories on the
evolution of human sexuality, which treat loss of estrus as a species-typical
characteristic, neither fully take into account nor adequately address the
limitations of existing data.
Furthermore, we suggest that a ma.jor reason for the persistent view of
loss of estrus as a species-typical feature is the assurnption that compared
to nonhuman primates, the expression of human sexual behavior is less
influenced by hormones and more subject to cognitive and social factors.
This perceived change in the relative importance of physiological factors in
sexual behavior, if not viewed as a dichotomy, is often seen as a trend from
prosimians to humans that is linked to the degree of brain and. especially.
, Loss of Estrus in Human Evolution 419
cortical expansion. This view is expressed well by Loy (1987): “The primary
change from the prosimians to cercopithecoids and great apes was a shift
from strict hormonal control of attractiveness, proceptivity, and receptivity
to moderate hormonal control of all three factors plus the appearance of
situation-dependent proceptivity and receptivity. The ape-to-human shift in-
volved a further strong reduction in hormonal influence on all aspects of
female sexuality” (p. 190). In a similar vein, Frayser (1985) notes, “Phys-
iological triggers for sexual activities and expressions of arousal became
relatively less important as cortical control and choice . . . became more
dominant” (p. 56). Such perceived broad trends in primate sexuality, scaled
according to degree of encephalization or conscious control (see also Burley
1979), do not fit our emerging picture of the factors regulating primate sexual
behavior. As an alternative to this scala naturae view of primate sexuality,
following the perspective of Crews and Moore (1986), we propose examining
the relative contributions of physiological and environmental factors as the
outcome of adaptation by particular primate taxa to particular socioecol-
ogical conditions.
Finally, the concepts loss of estrus, continual sexual receptivity, and
concealed o\Bulation must be given much greater analytical attention than
they have received so far. For example, all three are frequently used inter-
changeably to describe heightened sexual activity throughout the menstrual
cycle. We will show, however, that both empirically and theoretically, these
phenomena are distinct and, in some instances, independent.
In addressing these concerns, we analyze the concepts of and theories
concerning loss of estrus and concealed ovulation in the light of relevant
studies of primate sexual behavior. We conclude that study sample and de-
sign limitations of available data on human sexual behavior in relation to
the menstrual cycle preclude any conclusion about what is species-typical
behavior or a unique evolutionary development.
II. “LOSS OF ESTRUS”
Definitions, Concepts, and Data
Estrus has been defined as ‘&. . , a relatively brief period of proceptivity,
receptivity. and attractivity in female mammals which usually, but not in-
variably, coincides with their brief period of fertility” (Symons 1979; p. 97).
As this definition suggests, estrus refers primarily to a set of behaviors that
is indicative of the female’s readiness to mate and that may or may not co-
incide with the time of ovulation. This distinction between behavioral and
physiological events is made more explicit in Daly and Wilson’s (1983) defi-
nition of estrus as “. . . a relatively delimited period of female sexual re-
ceptivity, a stage defined by that receptive behavior rather than by hormonal
or other physiological factors” (p. 216).
Too Many Answers, Too Few
Questions
Horst D. Steklis and Catherine H. Whiteman
Department of Anthropology, Rutgers-The State University of
New Jersey
Models addressing the importance of “loss of es&us” in human evolution assume that,
as part of a general trend among higher primates, endogenous hormonal fluctuations
have less influence on human female sexuality than cognitive and socioenvironmental
factors. The diversity of reproductive patterns among primate species is not satisfac-
torily explained as the outcome of evolutionary trends along dimensions such as brain
enlargement, behavioral flexibility, or relative independence of behavior from pbysi-
ology. Rather, the role of hormones and other factors must be viewed in the context
of species’ life history and ecological constraints. Human studies on the relationship
between the menstrual cycle and sexual behavior have been limited to Western women
in industrialized societies, which may not reveal evolved behavioral-physiological pat-
terns. Furthermore, available studies have yielded inconsistent results. No single pat-
tern emerges that can be said to characterize the human female, and no conclusion can
be reached regarding the relationship between cyclic hormonal fluctuations and sexual
behavior and, thus, whether human ovulation is concealed. Future studies are needed
that are methodologically improved and systematically document the interaction among
ecological, subsistence, social, and physiological variables.
KEY WORDS: Loss of estruc: Concealed ovulation: Primate sexuality: Menstrual
cycle: Evolutionary models: Hormones and behavior.
I. INTRODUCTION zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA
odels of the evolution of human sexual behavior often point
M
male-female
to the loss of estrus in women as one of the most important
events in human evolution.
of estrus is a consequence
pair bonding and cooperative
It has been proposed that the loss
of the following: 1) facilitation
male hunting (Campbell
Morris 1967; Pfeiffer 1969): 2) females trading sex for meat hunted by males,
of
1974;
which in turn led to the development of pair-bonds and increased paternal
certainty (Alexander and Noonan 197X: Fisher 1982; Hill 1982: Lovejoy
Received July IS, 1988: revised March 23. 1989
Address reprint requests to: Horst D. Steklis. Ph.D.. Department of Anthropology. Rutgers-
The State University of New Jersey. Douglass Campus. New Brunswick, NJ 08903.
Ethology and Sociobiology IO: 4 17-434 ( 1989)
r<j Elsevler Science Publishing Co.. Inc.. IYXY
6.55 Avenue of the America\. New York. NY 10010
,418 H. D. Steklis and C. H. Whiteman
1981; Symons 1979: Zcveloff and Boyce 1982): 3) female opportunistic mat-
ing with a variety of males, thereby confusing paternity, increasing male-
female alliances, and reducing infanticide (Andelman 1987: Benshoof and
Thornhill 1979; Hrdy 1979; Tanner 1981): 4) avoidance ofconception because
of the risks, pain, and workload of pregnancy, childbirth. and infant care
(Burley 1979); 5) various structural/functional changes related to bipedalism
(Manson 1986; Spuhler 1978).
Many of these proposals have assumed that the human female is unique
among primates in exhibiting continuous sexual receptivity and no overt
clues to ovulation (e.g.. Benshoof and Thornhill 1979: Fisher 1982: Strass-
mann. 1981: Zeveloff and Boyce 1982); however. examination of sexual bc-
havior in comparative perspective has led primatologists to question the
uniqueness of human female sexuality (e.g., Gray and Wolfe 19X3: Hrdy
1979: 1986: Small 1988). For example, in discussing concealed ovulation,
Andelman (1987) observed that “. . concealed ovulation is so rare that it
is often incorrectly assumed to be restricted to human females, although it
also occurs among several other species within the order Primates” (p. 785).
Similarly, a review of patterns of primate sexuality led Hrdy and Whitten
(1986) to conclude that the traditional dichotomy between humans and other
primates in the display of sexual receptivity outside the time of ovulation
‘/
. . is an oversimplification. On the one hand, human females are clearly
not receptive all the time; . . On the other hand, the information . shows
many nonhuman primate females exhibit sexual receptivity outside the brief
period right around ovulation” (p. 384).
Nonetheless, concealed ovulation and continuous sexual receptivity t-e-
main key aspects of recent models of human evolution (Ember and Embet
19X4; Shaw and Darling 1984; Tooby and DeVore 1987; Turke 1984). The
problem with these models is that despite the use of a comparative per-
spective, they nevertheless inappropriately characterize human female scx-
ual patterns. For example, Manson (1986) argues for “the presence of a
bimodal pattern of elevated sexual arousability, with peaks in the premen-
strual phase and around ovulation at midcycle” (p. 21). As we will show,
this pattern of sexual activity is not necessarily a species-typical one. Morc-
over, presently available evidence does not permit the abstraction of any
single pattern of female sexuality. We propose that current theories on the
evolution of human sexuality, which treat loss of estrus as a species-typical
characteristic, neither fully take into account nor adequately address the
limitations of existing data.
Furthermore, we suggest that a ma.jor reason for the persistent view of
loss of estrus as a species-typical feature is the assurnption that compared
to nonhuman primates, the expression of human sexual behavior is less
influenced by hormones and more subject to cognitive and social factors.
This perceived change in the relative importance of physiological factors in
sexual behavior, if not viewed as a dichotomy, is often seen as a trend from
prosimians to humans that is linked to the degree of brain and. especially.
, Loss of Estrus in Human Evolution 419
cortical expansion. This view is expressed well by Loy (1987): “The primary
change from the prosimians to cercopithecoids and great apes was a shift
from strict hormonal control of attractiveness, proceptivity, and receptivity
to moderate hormonal control of all three factors plus the appearance of
situation-dependent proceptivity and receptivity. The ape-to-human shift in-
volved a further strong reduction in hormonal influence on all aspects of
female sexuality” (p. 190). In a similar vein, Frayser (1985) notes, “Phys-
iological triggers for sexual activities and expressions of arousal became
relatively less important as cortical control and choice . . . became more
dominant” (p. 56). Such perceived broad trends in primate sexuality, scaled
according to degree of encephalization or conscious control (see also Burley
1979), do not fit our emerging picture of the factors regulating primate sexual
behavior. As an alternative to this scala naturae view of primate sexuality,
following the perspective of Crews and Moore (1986), we propose examining
the relative contributions of physiological and environmental factors as the
outcome of adaptation by particular primate taxa to particular socioecol-
ogical conditions.
Finally, the concepts loss of estrus, continual sexual receptivity, and
concealed o\Bulation must be given much greater analytical attention than
they have received so far. For example, all three are frequently used inter-
changeably to describe heightened sexual activity throughout the menstrual
cycle. We will show, however, that both empirically and theoretically, these
phenomena are distinct and, in some instances, independent.
In addressing these concerns, we analyze the concepts of and theories
concerning loss of estrus and concealed ovulation in the light of relevant
studies of primate sexual behavior. We conclude that study sample and de-
sign limitations of available data on human sexual behavior in relation to
the menstrual cycle preclude any conclusion about what is species-typical
behavior or a unique evolutionary development.
II. “LOSS OF ESTRUS”
Definitions, Concepts, and Data
Estrus has been defined as ‘&. . , a relatively brief period of proceptivity,
receptivity. and attractivity in female mammals which usually, but not in-
variably, coincides with their brief period of fertility” (Symons 1979; p. 97).
As this definition suggests, estrus refers primarily to a set of behaviors that
is indicative of the female’s readiness to mate and that may or may not co-
incide with the time of ovulation. This distinction between behavioral and
physiological events is made more explicit in Daly and Wilson’s (1983) defi-
nition of estrus as “. . . a relatively delimited period of female sexual re-
ceptivity, a stage defined by that receptive behavior rather than by hormonal
or other physiological factors” (p. 216).
