Though we share an evolutionary history with primates, our species walked new

Transcription

1 Though we share an evolutionary history with primates, our species walked new and unique paths to arrive at our present existence. Our journey resulted in the acquisition of many novel and unique characters allowing us to survive, reproduce, and bequeath our individual traits to our children. Successful reproduction and relatively low mortality rates are critical to survivorship of a species. What reproductive characteristics has our species evolved and which most greatly shaped our evolution by conferring additional advantages in reproductive success and survivorship? Traits such as concealment of ovulation and loss of the estrus period in humans are odd considering our closest relatives who shares 98% of our DNA, chimpanzees, exhibit significant anogenital swelling during the ovulatory period of the menstrual cycle. These visual cues alert potential male mates about a female s curent fertility. By advertising the time they are most likely to conceive, females attract males for copulation. Copulation frequencies in chimpanzees and many other primate species peak during ovulation, with females mating constantly and often with multiple males. Copulation occurs at very low frequencies outside of the ovulatory period in these species. Why would obvious signs of likely conception times be selected against in humans? Concealed ovulation seems to necessitate frequent copulations to ensure insemination, since neither the male nor female would be certain when the ovulatory period occurred. Frequent copulation deprives participants of much-needed energy and wastes time that could have been used to perform more beneficial activities. This paper seeks the selective pressures in the history of human evolution ultimately resulting in the absence of anogenital swellings and the loss of estrus in our ancestral hominid women. 1

2 Female sexuality expresses itself through three indicators (Beach 1976). The first of these is pasive receptivity or a female s wilingnes to copulate with a male. Human females demonstrate constant receptivity through their wilingnes to copulate irrespective of the phase of the menstrual cycle. The second indicator relates to a female s active encouragement of a male to copulate, or her proceptivity. The third indicator is attractivenes which is a stimulus for excitation and ejaculation in males. The variation in receptivity, proceptivity, and attractiveness in most species depends upon the phase of the menstrual cycle in an individual female. These three indicators of female sexuality aid researchers in their quest to explain the female sexual traits of concealed ovulation and estrus loss. The three most popular hypotheses will be the discussion focus of this paper. THE PAIR-BONDING HYPOTHESIS Owen Lovejoy (1981) proposed the pair-bonding theory in his model of human origins. He utilizes the fossil record, primate observation and demographic evidence to distinguish five complexes uniquely indicative of humans: (1) a large neocortex, (2)bipedal locomotion, (3)reduced anterior dentition with molar dominance, (4) material culture, and (5) unique sexual and reproductive behavior. Lovejoy (1981) also asserts that bipedal locomotion directly enhanced reproductive fitness. In hopes of increasing reproductive success, late Miocene hominids were forced to modify factors affecting their survivorship and the amount of time between consecutive births (birth space). Lovejoy (1981) proposes reduction of birth space and increased survivorship through shifts in mating strategies as complimentary to inhabiting 2

3 new niches in the Pliocene. Brain expansion and material culture had not fully developed at this time and are consequently not responsible for shifts in reproductive strategies. The inefficient mother-infant relationship and constant injuries of infants from falling from their mother necessitated an increase in the parenting quality or quantity to improve survivorship of young dependents. (Lovejoy 1981). Because the mother foraged for herself and her offspring, constant travel with infant became a significant cause of infant death. If intensification of parenting allowed reduced mobility for females, infant mortality would be reduced as well. In this situation, Lovejoy (1981) argues polygynous social structures would not be selected, but rather pair-bonded monogamy would be favored. Through collecting and provisioning food for his mate and ofspring, a male s reproductive rate would increase. A female s ability to accommodate longer gestational and lactational periods would increase if her protein and calorie supply increased through male provisioning. Male provisioning helped achieve better dietary sources and increased allowance for more intense parenting necessitated by the tremendous length of infant dependency, which increased survivorship and reduced birth space. Lovejoy (1981) argued this would enable a progressive boost in the number of dependents in a group. If provisioning occurred, the use of hands to carry resources would be selected for and bipedality would emerge. Changes in skeletal morphology, especially pelvic and lower limb adaptation, would be strongly selected for due to the rapid exhaustion that bipedal locomotion causes in species which do not typically walk in this fashion (Lovejoy 1981). For male provisioning and monogamy to become characteristic of hominids, males could not be disadvantaged in securing mates. Morphological shifts in females 3

4 towards absence of visual signs of ovulation and the emergence of constant receptivity would further cement the pair-bond between a male and female. Increased copulation in a pair-bonded couple would help ensure conception and act as a social display asserting the couple s bond (Lovejoy 1981). Human females would become continually receptive to allow for increased copulation and the resulting paternity assurance of a male, eliminating the need for an externally obvious display of estrus. Lovejoy (1981) argued selection for pair-bonded males as their energetic ability to provision, improve survivorship, and copulation rate became better exploited. Assuming the emergence of pair-bonds was fundamental to hominid sexual strategy, any physical trait that reinforced monogamy would be favored by selection. Shifts towards monogamy would imply that males became directly interested in the survivorship of their offspring, leading to an early version of modern nuclear families (Lovejoy 1981). INFANTICIDE HYPOTHESIS Sarah Hrdy proposed the infanticide hypothesis to account for female sexuality. The behavior of males influences the fitness and survival of infants. Any sort of male behavior directly harming one of his offspring would be selected against. Langurs receive limited opportunities to mate with several males as they live in uni-male group systems (Hrdy 1981). Even though male langurs constantly observe female activities in the group, females might find multiple male mating advantageous enough to actively pursue (Hrdy 1981). Mating with multiple males may reduce the possibility of future male attacks against the mother and her offspring, if paternity confusion exists. Survival of future 4

5 offspring could be improved by a female if she mated with many males such as resident males and possible attackers and usurpers. This behavior occurs in groups with regular occurrences of infanticide such as langurs in uni-male troops and chimpanzees in multimale troops (Hrdy 1981). Conspicuous swelling could be detrimental to seeking copulations with outside males due to the surveillance of the male group leader, who would notice swellings indicating ovulation. Through situation-dependent receptivity resulting in concealed ovulation, females would not only be able to conceal likely times of conception but also confuse paternity. A male would be less likely to kill an infant if he was possibly the father. Wild langur females actively seek copulation with new males who have hostilely taken over her group (Hrdy 1981). If male-male competition potentially endangered females and their offspring, situation-dependent receptivity and concealment of ovulation could be advantageous for females. The evolution of concealed ovulation and more flexible receptivity might have increased the possibility of male assistance in situations of intergroup interaction or territorial defense (Andelman 1987) in addition to discouraging aggressive male actions against the infant. NON-SEXUAL SELECTION HYPOTHESIS Boguslaw Pawlowski (1999) takes a novel approach to the question of concealed ovulation and constant receptivity in humans, by proposing their evolution was not related to sexual selection but environmental stresses and cultural behaviors. He is primarily concerned with the assumptions that absence of ovulation is specific to humans and that constant receptivity is unique to humans (Pawlowski 1999). He suggests 5

6 replacing the chimpanzee model that is typically used in discussion of evolution with a model of relatively slight swellings in early hominoids (Pawlowski 1999). Possible causes for the sexual behavioral differences between humans and primates might be nothing more than side effects of morphology, ecology, and cultural features. Concealment of the visual signs of ovulation could be caused by bipedalism, water accumulation costs, hyperaemia of the area where swellings occur, an increase in adipose tissue, or olfaction serving as an effective announcement of likely conception times (Pawlowski 1999). Constant receptivity might be associated with increasing androgen levels related to increased endurance for walking or pursuit of prey (Pawlowski 1999). In many primate species, females allow copulation in most phases of the menstrual cycle; an intensification of sexual behavior is still often associated with the ovulatory phase (Pawlowski 1999). If constant receptivity means constant sexual activity of a female across her menstrual cycle, it might not be a distinctive feature of Homo sapiens. If this is so, proceptivity and attractiveness would differentiate Homininae from other primates. Proceptivity studies of women indicate similarities with other primates in the dependence of proceptivity on the phase of the menstrual cycle (Pawlowski 1999). Measurements of attractiveness could be increases in male sexual excitation evident by a reduction in time before ejaculation. Rhesus monkeys on average ejaculate after 5.4 minutes during the proliferative phase (occurring immediately before the ovulatory phase) and 12.5 minutes during the luteal phase, implying males respond to variations in attractiveness with faster ejaculation during the ovulatory phase, probably due to the female s increased atractivenes at this time (Pawlowski 1999). 6

7 Distribution of sexual activity independent of hormonal factors could result from ecological and/or cultural issues. In limited space reproductive behavior of males is greatly affected. The presence of other males typically increases sexual activity independently from the female menstrual cycle (Pawlowski 1999). Proceptivity and attractiveness might initially reduce the distance between males and females, resulting in the formation of couples. Conditions requiring animals to constantly spend time together reduces the significance of variability in proceptivity and attractiveness (Pawlowski 1999). The evolution of Homininae occurred during many periods of climactic change, which made flexible behavioral responses more adaptive. An increased independence of endocrine system function from the environment might have relaxed the rigid hormonal control over human behavior (Pawlowski 1999). The disappearance of visual sexual swellings might be a side effect of the evolution of bipedalism. As the shift to erect posture occurred, the position of female genitalia were relocated between the legs, rendering sexual swelling signals more costly (Pawlowski 1999). Erect posture changed the vision line of men so that female swellings would no longer be in the direct line of vision (Pawlowski 1999). As environmental changes occurred, more open-savannah environments appeared, rendering Homininae very susceptible to predators which would increase population densities. The long distance function of large sexual swellings would be lost in this context (Pawlowski 1999). Sexual swellings also increase the weight of a female which would increase her energetic requirements for bipedalism during periods of swelling. A savannah environment might have selected for water conservation and swelling typically requires an extra 1.5 liter of water for chimpanzees (Pawlowski 1999). Sexual swellings might 7

8 have resulted in inefficient evaporation of sweat (Pawlowski 1999). Sexual swelling might also have increased the risk of hypothermia at night due to the loss of heat through the hyperaemic sexual swellings (Pawlowski 1999). Ultimately Pawlowski (1999) felt that constant receptivity is not specific to our species and does not necessitate specific social structure or reproductive strategy. The absence of visual signs of ovulation could allow greater flexibility in choosing an adaptive reproductive strategy. The substantial plasticity of reproductive strategy might reveal that evolutionary selective pressures towards rigid social structures were absent (Pawlowski 1999). The pressures of a changing environment were probably substantially more important in the hominization process (Pawlowski 1999). PROBLEMS FOR THE PAIR-BOND HYPOTHESIS Lovejoy s (1981) analysis of the hominization process presents multiple problems, rendering this hypothesis very dubious. One major isue is Lovejoy s assumption that great apes required a shift in behavior due to the imminent possibility of extinction (Isaac 1982). Another concern is Lovejoy s (1981) explanation of human female sexuality as a result of a history of pair-bonds during early hominization. Flexibility in the distribution of sexual activity occurs in many Old World monkeys and apes (Pawlowski 1999) and its evolution through the social structures of monogamy and the nuclear family is highly doubtful (Harley 1982). Lovejoy (1981) also asserts that constant sexual receptivity and concealment of ovulation were necessary to facilitate pair-bonds. Near the time of ovulation, human females do demonstrate higher frequencies of sexual behavior (Pawlowski 1999; Hrdy 1981). There is also no evidence 8

9 implying increased copulation or attraction maintains pair-bonds between mates (Harley 1982). Lovejoy (1981) does not discuss the possibility of hominization occurring in a polygynous mating structure, despite strong evidence from the archaeological record. Early hominids were sexually dimorphic, which is usually accounted for by male competition in a polygynous society. Sexual dimorphism is not explained in the context of monogamy. Lovejoy (1981) proposes the idea of a home base from which females ranged outward to find food which is not supported by current patterns of chimp behavior. Lovejoy also assumed that in nature, females reproduce at rates near their physical capabilities, reducing natural selection. A variance in female reproductive success does exist. Senior wives in polygynous arrangements often possess more nutritious diets, decreased amounts of physical exertion, as well as lower psychological stress (Hrdy 1981). These advantages and others might have resulted in fertility differences in females. Phylogenetic analysis were performed to demonstrate relationships between concealed ovulation and mating systems in anthropoid primates (Sillen-Tullberg; Moller 1993). Mating systems were divided into (1) monogamous, (2) uni-male, and (3) multimale; and, visual signals of ovulation were considered (1) absent, (2) slight with pinkness of external genitalia, and (3) sexual swelling/skin which could be seen from a distance. Results indicated the absence of ovulatory signs evolved a total of 8-11 times, with 2 of those occurrences taking place in Hominoidea (Sillen-Tullberg; Moller 1993). 9

10 Monogamy was the least common mating system, evolving three times in Platyrrhini and 4 times in Catarrhini (Sillen-Tullberg; Moller 1993). Ovulatory signs were lost under monogamy only 0-1 times. In the absence of visual signs of ovulation, monogamy evolved 4-6 times and in the presence of swellings, monogamy evolved 1-3 times (Sillen- Tullberg; Moller 1993). These results indicate that monogamy was an unlikely ancestral state for the evolution of concealed ovulation. Perhaps the presence or lack of visual cues of ovulation influences mating systems, as opposed to mating systems influencing the appearance or disappearance of ovulatory signs (Sillen-Tullberg; Moller 1993). Sillen- Tullberg and Moller (1993) also suggest that the function of nonexistent ovulatory signs has changed. In the past this trait might have been useful for paternity confusion but it has moved towards increasing paternity certainty in males. The absence of ovulatory signs is an important, but not essential, requirement for the evolution of monogamy (Sillen-Tullber; Moller 1993). PROBLEMS FOR THE INFANTICIDE HYPOTHESIS The idea that infanticide occurs at any degree of constancy concerns many researchers who feel that Hrdy (1981) made an assumption before examining the evidence and consequently made her data fit that asumption. Most of Hrdy s (1981) research involved Hanuman langurs, but many other researchers disagree with the conclusions she drew about infanticide. The earliest accounts of infanticide in Hanuman langurs matriculate from Dharwar India and there is only one instance in which a usurper was directly observed to kill an infant (Bartlett; Sussman, and Cheverud 1993). All other cases of infanticide were not observed first hand but rather indirectly inferred. 10

11 There are problems with Hrdy s data (1981) from her research at Mount Abu India. She reports five group takeovers with many suspected cases of infanticide. These infanticide attacks were seldom directly observed by Hrdy or her research team (Bartlett, Sussman, and Cheverud 1993). She usually was informed of infanticide by locals claiming to have witnessed the acts. Hrdy s (1981) model predicts that males will not kill related individuals, interbirth intervals will decrease in infant deprived females, usurpers will inseminate the infant deprived female, and infanticidal males will gain a reproductive advantage relative to noninfanticidal males. Questions have arisen regarding an infanticidal male s ability to distinguish and resolutely eliminate offspring that he did not sire. This is further confounded with research suggesting that infanticidal attacks usually occur in a context of generalized intersexual and intrasexual aggression (Bartlett, Sussman, and Cheverud 1993). Intersexual aggression during infanticidal attacks often resulted in attacks on adult females, adult females and juveniles, and adult females that were cycling; repeated atacks on a female after her infant s death occurred as well (Bartlett, Sussman, and Cheverud 1993). The heritability of infantcidal behavior is still problematic and the possibility exists that if infanticidal behavior can increase a male s fitnes, such increases could be attributed to other correlated traits, like aggression levels (Bartlett, Sussman, and Cheverud 1993). If this is true and a phenotypic relationship exists between infanticide and higher overall aggression levels, infanticidal males may seem fit even though their fitness may or may not be higher than noninfanticidal males (Bartlett, Sussman, and Cheverud 1993). Future research must examine if the sons of infanticidal males are more 11

12 likely to become infant killers than the rest of their population and if they will have the opportunity to express their infanticidal behavior. SUPPORT FOR THE INFANT KILLING HYPOTHESIS C. Borries et al (1999) used DNA analysis of Hanuman langurs to determine that infanticide is adaptive in langur monkeys. A study of 18 wild groups of Hanuman langurs revealed that if an infant died, the mean interbirth interval of 2.4 years did become shorter. DNA was removed from the feces of the langurs and five loci were used to make paternity exclusions. There were 35 observed or assumed cases of infanticide and researchers obtained complete sets of fecal samples from 16 of the 24 male-infant pairs involved in attacks (Borries and others 1999). In all 16 cases, DNA analysis allowed for the exclusion of the aggressive male as the father of the attacked infant; the infants sired by infanticidal males were never killed or even attacked (Borries and others 1999). Males also seem to gain an advantage from infanticide by shortening birthspace and reproducing with the infant-less mother. DNA profiling revealed that in the four tested cases infanticidal males sired the next offspring of the victim s mother (Bories and others 1999). The evolution of concealed ovulation in vervet monkeys has been well documented, and the proposed theory explaining this is consistent with Hrdy s (1981) infanticide theory. Sandy J. Andelman (1987) presents quantitative evidence implying wild female vervets do exhibit concealed ovulation. Andelman (1987) monitored ovarian function by collecting urine from adult females three times a week for two years during 12

13 the vervet s breeding season. Ovarian function and placental function in vervets was measured by testing for urinary pregnanediol-3α-glucuronide, a progesterone metabolite. Conception dates were inferred by backdating estimates from known dates of birth and a gestantional length of 163 days (Andelman 1987). No evidence was found for the exhibition of visual signs of ovulation in female vervet females. Studies of vervet copulation revealed that before conception and sometimes the beginning of the ovarian cycle vervets engaged in sexual activity; 57.5% of all females continued sexual activity throughout the first half of pregnancy (Andelman 1987). Within the male dominance system, the top 1/3 acquired significantly more mates as compared to the bottom 2/3 of the hierarchy; however, the top, middle, and bottom groups received 31.5%, 37%, and 31.5%, respectively, of copulations during the week most likely to result in conception (Andelman 1987). Vervets have high rates of male takeovers, usually occurring during the breeding season. This evidence suggests that within the vervet species concealed ovulation benefits females by its ability to decrease the occurrence of infanticide (Andelman1987). The Sillen-Tullberg and Moller (1993) research indicates that the ancestral mating system of humans was probably a harem holder. Their research also suggested that multi-male reproductive structure is likely to have evolved independently in the chimpanzee lineage. Loss of visual signs of ovulation is assumed to have occurred 3-7 times under uni-male systems and 3-6 times under multi-male systems (Sillen-Tullberg and Moller 1993). PAWLOWSKI ON FEMALE SEXUALITY 13

14 Pawlowski (1999) argues that constant receptivity in human is not unique, many other primates exhibit constant receptivity. Noncyclical receptivity occurs among langurs, which lack substantial male-investment and solitary apes such as the orangutan may copulate at any time in the reproductive cycle (Hrdy 1981). Female chimpanzees and bonobos will also mate regardless of the phase of the menstrual cycle (Pawlowski 1999). Pawlowski (1999) also asserts that the human female distribution of sexual activity is related, in a small degree, to the phases of the menstrual cycle. Since differences in receptivity may be only quantitative as opposed to qualitative, Pawlowski believes constant receptivity is not a distinctive feature of Homo sapien. Constant receptivity is the defining feature in Lovejoy s (1981) pair-bond hypothesis and is incorporated into Hrdy s(1981) explanation of concealed ovulation. If constant receptivity is not unique to us, it should not be used to explain morphological adjustments in our evolutionary history (Pawlowski 1999). He furthers his argument by claiming that there was no real uniqueness in the proceptivity and attractiveness indicators in females either, and that sexual selection could not have been directly acting to conceal ovulation in hominid females (Pawlowski 1999). PAWLOWSKI AND OLFACTION Pawlowski (1999) argues that the loss of visible external signals of ovulation does not equate with complete concealment of ovulation, suggesting that olfaction could have discerned times of ovulation during hominization. Studies on rhesus monkeys demonstrated that in females the secretion of copulins, parts of vaginal secretion with strong smells, during ovulation can assist in alerting males about times of likely 14

15 conception (Stoddart 1986). The males are able to associate the smell of copulins with ovulation and are often seen inspecting a vagina with these secretions immediately before copulation. (Stoddart 1986). This is consistent with Hans Kummer (1968) field study of Hamadryas Baboons, in which males were known to inspect and touch the vaginas of females before copulation. Only the Lemuridae of the prosimian family have more apocrine scent glands than humans. Accumulation of apocrine glands constitutes distinct organs such as the axillary organs, secreting smell from early puberty to old age. However, no function has been attribute to the axillary organs of humans (Stoddart 1986). DISCUSSION Most current understandings of human evolution and origin may strongly disagree with Lovejoy s (1981) hypothesis that maintenance of the pair-bond is facilitated through continual receptivity and the concealment of ovulation which was necessary to secure adequate food provisioning from a male to keep her and her offspring healthy. Lovejoy (1981) appears to equate being constantly receptive with the ultimate loss of signals of ovulation. Hrdy (1981) has a fairly strong argument for the concealed ovulation in humans. Her model accounts for constant receptivity s presence in other species and suggests concealment of ovulation is not entirely unique to humans. She still appears to associate a shift towards constant receptivity with concealment of ovulation. Much support has been garnered for this hypothesis, but the biases present in her and other primatologists field work should not be forgotten. There are many factors influencing infant mortality 15

16 and several of the asumed cases of infanticide could be equaly explained by other non-sexually selected pressures. More research on the heritability of infantcidal behavior needs to be performed on a large scale level. The proposal that infanticide is only a corollary of the advantageous higher aggression levels present in some males seems reasonable. Being a dominant usurper male may increase male fitness and behaving in infantcidal manners could be a part of the phenotype of these powerful males. Pawlowski s (1999) ideas on concealment of ovulation were very intriguing. Even if the entire article is incorrect, it should be appreciated as an effort to step away from the window through which we have longed viewed hominization. He makes some very interesting distinctions about constant receptivity: that humans are not unique in being constantly receptive, but that we also are not completely independent of the hormonal system regulating the menstrual cycle (Pawlowski 1999). His argument against sexual selection hinged on the existence of no real uniqueness in the indicators of human sexuality in relation to nonhuman primates. Unfortunately many of his ideas will be very difficult to examine. Research on olfactory and hormonal regulation of behavior is very difficult to perform. Pawlowski (1999) also basis several of his suggestions on research being performed on contemporary women. One must be careful when extrapolating present day understandings of cultural factors to historical explanations. 16

17 Female Sexuality and the Evolution of Concealed Ovulation with Constant Receptivity Casey Adams 23 February 2005 Text: 16 pgs References Cited: 2 pgs 17

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