Genetic influence on the expression of hand preferences in chimpanzees (Pan troglodytes): evidence in support of the right-shift theory and developmental instability.

Genetic mechanisms have been proposed to explain the pervasive representation of right-handedness in humans, whereas random, nongenetic factors have been posited to explain the lack of population-level right-handedness in nonhuman primates. We report evidence that hand preferences in chimpanzees are heritable, even among related individuals raised in different environments. Furthermore, we report that the degree of heritability is modified by factors associated with developmental instability, notably, offspring parity. The data are interpreted to reconcile both genetic models for handedness and hypotheses suggesting that developmental instability influences variation in handedness.

Birth order and left-handedness revisited: some recent findings in chimpanzees (Pan troglodytes) and their implications for developmental and evolutionary models of human handedness.

This paper examines the relationship between parity, pregnancy outcome, and handedness in a sample of captive chimpanzees (Pan troglodytes). The relation between parity, maternal age and positive or negative pregnancy outcome was assessed from life history data for 536 chimpanzees housed at the Yerkes Regional Primate Research Center. The incidences of negative pregnancy outcome (notably spontaneous abortions and stillbirths) were significantly higher in parities of 8 or higher compared to all other parities. In a sub-sample of 165 chimpanzees, the relation between parity, maternal age and handedness was assessed to determine whether left handedness may serve as a marker of prenatal pathology. These analyses indicated that left-handedness was more prevalent in 1st and 8 or higher parities compared to parities between 2 and 7, respectively. Possible prenatal hormonal and periparturitional factors are discussed as possible mechanisms for the observed findings.

Birth order and hand preference in chimpanzees (Pan troglodytes): implications for pathological models of handedness in humans.

The effect of birth order on hand preference was assessed in a sample of 154 captive-born chimpanzees. Subjects were classified as first, middle, or latter born using 2 classification criteria based on their birth order. Hand preference was measured using a task that elicited coordinated bimanual actions. Significant birth-order effects were found for both classification criteria, with first- and latter-born subjects exhibiting a lesser degree of right-handedness compared with middle-born subjects. These data suggest that biological rather than sociological factors play a greater role in explaining the observed birth-order effects on hand preference in humans.

Perineal swelling during pregnancy in common chimpanzees and puerperal pathology.

Perineal swelling during pregnancy in captive common chimpanzees (Pan troglodytes) was studied to examine if the swelling pattern is consistent with known fluctuations in estrogens and progesterone and to test associations between reduced swelling and pathological outcome. Analyses of swelling during 107 pregnancies with a variety of outcomes revealed that a majority of swelling patterns fit an endocrinological model closely, but that a small minority (6.6%) from low parity mothers had exaggerated and extended swelling, suggesting an altered sensitivity of the swelling to steroids. Disregarding this extreme minority, swelling was found to be significantly reduced from that of normal outcome pregnancies for sub-groups with varying degrees of maternal incompetence, neonatal fatality, and stillbirth. This reduction was most marked for pregnancies in nursery-reared mothers. Given the validity of the correspondence between swelling patterns and steroid concentrations, lower estrogen concentrations are implicated in the etiology of the puerperal pathologies seen. That steroid hormone concentrations during pregnancy may influence maternal behavior in apes provides a clue to the etiology of post-partum depression in women.

Sexual behavior of chimpanzees (Pan troglodytes): male versus female regulation.

We investigated the sexual behavior of 13 chimpanzees (Pan troglodytes) in 2 types of pair test in order to clarify the interaction of social variables with female hormonal state. The frequency of copulation in tests in which the partners were freely accessible to each other was related to the male's dominance over the female; copulation was less frequent and was related to social compatibility in tests in which the female controlled access. Copulation was related to female hormonal state in both types of test. The results demonstrate (a) an association between female hormonal state and sexual activity of chimpanzees, (b) the influence of social relationships on sexual interactions, and (c) the importance of focusing on female sexual behavior before copulation, rather than copulation per se, in research on sexual arousability of female primates.

Effects of an oral contraceptive on sexual behavior of chimpanzees (Pan troglodytes)

Behavioral and physiological effects of a combined oral contraceptive (OC) were studied in chimpanzees for comparative purposes related to (i) the ambiguity surrounding the effects of OCs on the sexuality of humans, (ii) the close biological relationship between chimpanzees and humans, especially with respect to endogenous sex hormones and sexual behavior, and (iii) the relatively greater behavioral sensitivity of the chimpanzee to changes in sex hormone levels such as those that accompany the use of OCs. Two different types of pair tests and detailed behavioral assessments were used to differentiate the hormonal effects of female behavior from social effects imposed by the male. Anogenital swelling and copulation were reduced during OC cycles, but the effect of the OC on copulation was directly related to the social and sexual relationship of the pair during natural cycles. The more compatible and more frequently copulating pairs in the natural cycles continued to copulate during the OC cycles, albeit at reduced rates, whereas the less compatible and less frequently copulating pairs ceased copulating altogether when the female received the OC. There was no independent effect of the OC on ejaculation per se. Both male and female sexual initiative were reduced in the OC cycles, but female responsiveness to male sexual solicitations and direct copulatory attempts were not affected. Data indicate that despite generally adverse effects of the OC on certain physiological and behavioral dimensions of sexuality, social factors ultimately determined the degree of response to the OC.(ABSTRACT TRUNCATED AT 250 WORDS)

Serum and urinary concentrations of sex hormones and genital swelling during the menstrual cycle of the gibbon.

The relationship between sex hormone concentrations and female genital swelling during the menstrual cycle in the monogamous gibbon was comparable with that of polygamous female primates, such as the chimpanzee, which live in multimale groups and have larger swellings. The data, therefore, support the hypothesis proposed by C. R. Carpenter more than 50 years ago, that the gibbon's genital swelling, like that of other female primates, reflects basic physiological processes associated with progress of the menstrual cycle. Genital swelling increased during the follicular phase with increasing concentrations of oestradiol and oestrone glucuronide, reached maximal swelling in association with the mid-cycle peaks in the oestrogens and LH and began detumescence with the initial increases in progesterone during the luteal phase. The data also suggest that the menstrual cycle of the gibbon is shorter than previously reported, since cycles of 19-22 days exhibited hormone patterns that are consistent with ovulation. The genital swelling of the female gibbon is a useful marker for monitoring progress of the menstrual cycle and the presumptive time of ovulation.

Testicle size of orang-utans in relation to body size.

Few data are available for assessing the relative testicle size of orang-utans, Pongo pygmaeus, so measures were obtained for 31 individuals of varying age. It was shown that the volume of the testicles, calculated from in situ measures of testicle length and breadth, closely approximates testicle weight when multiplied by the specific gravity of solid tissue. Growth curves for body weight and data published for wild specimens were evaluated to obtain the weight most characteristic of male Pongo, and the ratio of testicle weight to body weight was calculated. The mean ratio for individuals with fully adult stature is 0.034, similar to but smaller than that of humans at about 0.050, and larger than the ratios reported for 5 gorillas at 0.013. The testicles mature faster than the body, however, so the mean ratio for young adult orang-utans is about 0.056 and resembles the ratio for humans more closely than the full adults. The differences between the ratios for a monogamous gibbon species, orang-utans, and humans is accounted for when testicle size relative to the weight of the female is considered. This is consistent with a sperm dilution effect produced by variation in the size of the female reproductive tract. The small relative testicle size of the gorilla is anomalous and requires verification as does the application of female size to scale the testicles.

Hormone levels and anogenital swelling of female chimpanzees as a function of estrogen dosage in a combined oral contraceptive.

A combined oral contraceptive consisting of ethinyl estradiol (EE2) in three dosages (50, 100, and 400 micrograms) and norethindrone (0.5 mg) was given to female chimpanzees to determine the effect on endogenous sex hormone levels and anogenital swelling. Serum levels of EE2 increased with increasing dosages of EE2, estradiol decreased, and luteinizing hormone, progesterone and testosterone were maintained at approximately midfollicular phase levels. Urinary levels of EE2 glucuronide increased with the increasing dosages of EE2, whereas estrone and pregnanediol glucuronide were essentially undetectable. The cyclic increase in female anogenital swelling was abolished when the norethindrone was combined with 50 micrograms of EE2 and relatively constant and low levels of swelling were recorded. Relatively constant but successively higher levels of swelling were recorded when the norethindrone was combined with the higher dosages of EE2. These effects of oral contraceptives on female genital tissues are relevant to our laboratory studies of sexual behavior in chimpanzees given oral contraceptives and could also have implications for women taking oral contraceptives.

Genital swelling in females of the monogamous gibbon, Hylobates (H.) lar.

Cyclical changes in the vulvae of five adult lar gibbons (Hylobates [H.] lar) were studied and compared with those of eight lowland gorillas. The results reveal that the gibbons have relatively conspicuous and specialized sexual swellings that alter shape and appearance during the ovarian cycle. At maximum extent, the genital swellings of gorillas are relatively and absolutely smaller than those of gibbons, and lack the distinctive coloration seen in the genital swellings of the smaller apes. We conclude that the female gibbon's sexual swelling is a far more conspicuous and effective signal of estrus status than that of the gorilla, and that this is not explicable in terms of allometry. Previous investigators have pointed to one-male mating systems, monogamous pair-bonding, or an arboreal habitat as reasons that some primates should have less conspicuous signals of estrus than others. Our findings for the gibbon are the reverse of these predictions, and indicate that sexual selection other than by intermale competition for estrous females is implicated in the ultimate causation of the gibbon's swelling. The adaptive value and significance of the female gibbon's sexual signals remain unclear, however.

The external genitalia of female gibbons, Hylobates (H.) lar.

The external genitalia of one perimenarcheal and five adult female white handed-gibbons (Hylobates (H.) lar) were examined to clarify their gross anatomy. It was found that the vulval structures were complex and exhibited inter-individual variation in arrangement. This complexity appears to result from an ontogenetic process by which the tissues of the vaginal rim (the labia minora) bud-off and extrude extensions toward the vagina immediately prior and subsequent to menarche. Two of these lobular structures surround the urethral meatus and constitute a urethral eminence. The tissues of the vulva, excluding the clitoris with associated prepuce and frenulum and vestigial labia majora, undergo cycles of tumescence and detumescence during intermenstrual intervals. The complex form of the external genitalia and the presence of a swelling cycle are unusual for a monogamous species, are contrary to current applications of sexual selection theory, and raise questions about the significance of mate choice in hominoid evolution.

Assessing variation in the social behavior of stumptail macaques using thermal criteria.

This paper reports a method for comparing the environments of nonhuman primates based on biophysical, thermal criteria. The method is applied to an analysis of behaviors exhibited by group-living stumptail macaques (Macaca arctoides), documented by a group-scan observation technique, to test the hypothesis that the expression of social behavior is dependent on thermal conditions. Thermal conditions are identified by considering sky cover and the relative cooling power of the environment. The results show that the rates of occurrence of affiliative, play, and solitary behaviors are altered significantly at a relative cooling power at or above 550 kcal/m2/hr under cloudy conditions and at or above 600 kcal/m2/hr under sunny conditions. In addition, the rates of occurrence of play, sexual, aggressive, and submissive behavioral states are also significantly different under cloudy, rather than sunny, conditions over particular ranges of cooling. It is possible to conclude that thermal criteria affect the expression of social behaviors by stumptail macaques. This is consistent with studies of huddling behavior exhibited by stumptail macaques and rhesus macaques (M. mulatta), and suggests that 1) certain changes in the expression of social behaviors may be thermoregulatory in at least some nonhuman primate species and 2) thermal criteria are likely to be useful tools when conducting comparative analyses of behavioral data collected on animals in outdoor environments.

The external genitalia of female pygmy chimpanzees.

The external genitalia of four adult female pygmy chimpanzees (Pan paniscus) were examined during a 2-year period. It was found that the labia majora are retained in adults of this species and that, when tumescent, the labia minora effectively relocate the frenulum and clitoris so that they point anteriorly between the thighs. When detumescent, the configuration of the labia minora and clitoris resembles that of immature common chimpanzees (P. troglodytes). It is suggested that the simple, structural relocation of the clitoris from the normal condition noted in adult P. troglodytes makes possible the homosexual, intergenital rubbing observed in P. paniscus, when ventroventral juxtaposition of the individuals permits eye-to-eye contact. In addition, this change probably increases sexual stimulation of the female during heterosexual, ventroventral copulations. The possibility of intense, face-to-face sexual interactions has been achieved by P. paniscus without the evolution of bipedalism and the consequent reorientation of the genitalia seen in Homo sapiens.