The Oestrus That Never

'The Impetus, the Lyrical oestrus, is gone.'

Fitzgerald

A recurrent theme in discussions about the origins of human sexual behaviour concerns the concept of oestrus, as it applies to female mammals, and to the presumptive loss of oestrus during human evolution. Oestrus, as originally defined by Walter Heape (1900), denotes a period of heightened sexual activity in female mammals, in association with the likelihood that ovulation will occur and that mating will result in conception. Heape noted that 'it is during oestrus, and only at that time, that the female is willing to receive the male.' The term derives from the Greek word for the gadfly, whose bite drives animals into a frenzy; the implication being that females are in a state of sexual frenzy or in heat during oestrus. Ovarian hormones (and especially oestrogen and progesterone) control the onset and duration of oestrus, so that ovariectomy is usually associated with loss of the female capacity to display sexual receptivity in many mammals. This is the case, for example, in rodents such as the rat, in carnivores (e.g. the cat and ferret), in rabbits, ungulates (such as cattle and sheep), and in many others. It is not, however, a universal attribute, applicable to all mammalian groups or species.

The choice of terminology can have profound effects upon the progress of science, just as in other areas of human affairs. Clearly, women do not come into heat; nor do they display a restricted period of sexual interest and receptivity when ovulation is likely to occur. Human sexual behaviour differs in important ways from the behaviour that occurs during the restricted oestrous periods of rats, sheep, and dogs. In human beings, copulations may take place throughout the monthly menstrual cycle, after ovarian cycles cease at the menopause, or as a result of ovariectomy. This is not to imply that the menstrual cycle and ovarian hormones have no effects upon human sexual behaviour; I shall return to this subject later in this chapter. However, since women do not experience circumscribed periods of sexual receptivity, anthropologists have sought to explain how and why, there has been loss of oestrus during human evolution. Nor is it obvious when ovulation is likely to occur during the human menstrual cycle, as women do not exhibit external cues, such as the oestrogen-dependent sexual skin swellings found in chimpanzees and some Old World monkeys. Thus, in addition to searching for the reasons why oestrus was lost in human ancestors, scientists have sought to explain the origins of concealed ovulation. Symons (1979), for example, proposed that 'estrus was lost some time after humans last shared a common ancestor with any living non-human primate'. This would mean that oestrus occurred in the common ancestors of Homo sapiens and the modern day African apes, and that it was lost during the evolution of the australopithecines or during the emergence of the genus Homo. A number of selective forces have been proposed to explain these events. It has been argued that loss of a circumscribed period of oestrus, or signals of impending ovulation, would have promoted pair bonding in human ancestors. Increased opportunities for copulation within the pair bond could have benefited male partners in terms of greater certainty that they had sired any resulting offspring. Such pair-bonded males might also have increased their fitness by providing greater resources to their mates and offspring; an important selective strategy given the relative helplessness of human infants, slow rates of development, and extended inter-birth intervals in the human species (e.g. Morris 1967; Alexander and Noonan 1979; Lovejoy 1981; Fisher 1982). It has also been posited that loss of oestrus and concealment of ovulation during human evolution might have provided females with increased opportunities to mate with additional males (i.e. to engage in extra-pair copulations), and thus to confuse paternity and reduce the risks that males might engage in infanticide (Hrdy 1981). However, the most peculiar line of reasoning that I have encountered in relation to explaining the concealment of ovulation during human evolution is due to Burley (1979). She advanced the hypothesis that concealment of ovulation would have prevented women from avoiding matings during the fertile period; their motivation for such avoidance would have been to prevent unwanted pregnancies and to reduce the (certainly large) physiological costs involved in pregnancy, childbirth, and post-natal care. Women who developed concealed ovulation were unable to identify the fertile period, and so could not choose to avoid copulation at that time; therefore, they produced more offspring and passed on more of their genes to future generations.

The notion that sexual behaviour might play some cohesive role in primate social organization is not new. In The Social Life of Monkeys and Apes, published in 1932, Zuckerman advanced the view that 'reproductive physiology is the fundamental mechanism of society' and that 'the main factor that determines social grouping in sub-human primates is sexual attraction.' Zuckerman thought that monkeys and apes are sexually active all year round, or at least that the sexes are held together by sexual attraction throughout the year. This was postulated to be the physiological and behavioural basis of group life. Subsequently, it became clear that some monkey species exhibit distinct mating seasonality (as reviewed by Lancaster and Lee, as early as 1965). Yet the absence of sexual activity for large periods of the year did not preclude these monkeys from living in permanent social groups. It is peculiar that despite evidence amassed from a burgeoning program of field studies of the non-human primates conducted during the 1960s and 1970s, Zucker-man refused to change his viewpoint, which he reiterated and defended in the second edition of his book, published in 1981.

The ecological factors which might underpin the evolution of social groups in monkeys and apes were also beyond Zuckerman's scope; indeed, he stated that 'Lack of relevant information makes it impossible to discuss here the subject of the ecology of the primates' (Zuckerman 1932; 1981). Yet, research on primate behavioural ecology supports the view that the physical nature of the habitat, including the distribution of food (and seasonal fluctuations in its availability) has crucial effects upon the size and composition of social groups. Females, in particular, benefit from group membership if this enhances their ability to obtain resources for themselves and for their dependent offspring. Males, in turn, compete for access to females, which are a limiting resource in reproductive terms. As Wrangham (1979) encapsulated it, 'the entwined distribution of females and males yields the social system.' Thus, ecology and not just sexual attraction is likely to play a pivotal role in determining the sizes and compositions of primate groups. The same arguments apply to other mammals, as for example the social carnivores. As an example, lions form prides because the survival and reproductive success of individual pride members is enhanced by life within a social group. A group of lionesses is more successful than a single female could be, at holding territory, hunting larger prey, and rearing their cubs in communal 'creches'. Males compete in order to associate with a group of females, but sexual behaviour per se is not the reason that lions live in prides (Schaller 1972; Packer, Scheel, and Pusey 1990).

Although Zuckerman greatly over-estimated the importance of sexual attractiveness and sexual behaviour in relation to the origins of primate social organization, he made valuable observations on the menstrual cycle and noted its relationship to patterns of behaviour. Adult females of all the Old World monkey and ape species exhibit menstrual cycles which are physiologically homologous with the human menstrual cycle. Zuckerman noted that baboons, macaques, and other monkeys tend to engage in sexual activity most frequently during the first half (follicular phase) of the monthly cycle, including the peri-ovulatory period, rather than during the second half (luteal phase) of the cycle. He was clear that these were not oestrous cycles, as females were 'ready to accept the advances of the male at all times, whereas the female lower mammal will mate, as a rule, only at those isolated intervals when she is in the physiological state of heat'.

Clearly, such observations should have constituted a major challenge to the development of theories about the origins of human sexuality, couched in terms of some unique loss of oestrus in the evolutionary lineage which produced Homo sapiens. It appears more likely that oestrus was lost in the common ancestors of the monkeys and apes, and not, as Symons (1979) proposed, after divergence of the hominid lineage from the common ancestors of human beings and the African apes. Indeed, a substantial number of publications has appeared over the years which critique the application of the concept of 'oestrus' to descriptions of sexual behaviour in the anthropoid primates, and some of these address the issue that absence of oestrus in women cannot be explained as a uniquely human trait (Rowell 1972; Hrdy 1981; Keverne 1981; Dixson 1983a; 1992; 1998a; 2001; Loy 1987; Goy 1992; Pawlowski 1999a; Martin 2003).

To emphasize the point about the importance of ecological factors as determinants of primate social organization and mating systems, and the absence of oestrus in anthropoids, I shall describe some field and laboratory observations of two African monkey species: the talapoin (Miopithecus talapoin) and the mandrill (Mandrillus sphinx). Both these species concentrate their copulatory activity within annual mating seasons, and both exhibit interesting shifts in social organization at such times. However, neither the talapoin nor the mandrill exhibits a peri-ovulatory oestrus of the type defined by Heape.

The talapoin is the smallest of the Old World monkeys; males weigh about 1.4 kg, and females just 1.0 kg when adult. Talapoins live in dense riverine rainforests in Cameroon and Gabon and occur in large multi-male/multi-female troops, commonly numbering more than eighty individuals (Rowell 1973; Rowell and Dixson 1975). Adult and sub-adult males form a distinct sub-group, and they do not mix extensively with the adult females except during the annual mating period. In Cameroon, the mating season occurs between the months of January to March, and occupies the longer of the two dry seasons which occur each year. Figure 6.1 shows monthly levels of rainfall in Cameroon at Mbalmayo, where these studies were conducted, together with data on the timing of talapoin mating and birth seasons. Interestingly, in northeast Gabon, where the dry and wet seasons are 6 months out of phase with those in South Cameroon, the mating season is also shifted by 6 months (June-August) with a birth season in December and January (Gautier-Hion 1968). Photoperiodic or temperature cues are most unlikely to account for these circannual rhythms of matings, conceptions, and births, which occur in equatorial environments. It is more likely that

JFMAMJJAS O ND Months

Figure 6.1 Seasonal patterns of reproduction in groups of talapoin monkeys (Miopithecus talapoin) in Cameroon. Monthly variations in rainfall correlate with annual cycles of mating behaviour (black bar) and births (open bar).

Source: Based on Rowell and Dixson (1975).

changes in nutritional or other factors secondary to seasonal shifts in rainfall trigger the neuroendocrine events which govern the start of the mating season. Female talapoins develop pink sexual skin swellings at this time, and it is suspected that social cues also play some role in the fine-tuning of their swelling cycles. Thus, in two troops of talapoins studied in Cameroon, females within each group showed much tighter co-ordination of their sexual skin swelling phases than was apparent between the troops, even though they occupied adjacent home ranges (Rowell and Dixson 1975).

During the annual mating season, males move from their subgroup to associate with females and to copulate; the extent of these movements and associations correlates strongly with the extent to which females have developed their sexual skin swellings (Figure 6.2). Females mate with multiple males, and there is a high level of aggression in the troop. Detailed observations of individual animals are exceedingly difficult to obtain because talapoins are small and live in dense forests. However, it is apparent that copulations occur over an extended period of the swelling cycle, and this conclusion is strengthened by the results of studies on captive groups of talapoins, which quantified changes in behaviour throughout the menstrual cycle (Scruton and Herbert 1970; Dixson et al. 1972). As can be seen from the results of these studies (Figure 6.3) matings occur throughout the follicular phase of the cycle, as the females' swellings enlarge due to oestrogenic stimulation, and are much less likely to occur during the luteal phase. There is no restriction of matings to the peri-ovulatory period, however, and no limitation of female sexual presentations or willingness to accept males in a period of heat or oestrus.

By contrast with the talapoin, the mandrill is a massive monkey and the adult males in particular are spectacular creatures, weighing more than 30 kg and adorned with red and blue sexual skin on the

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