Homosexual behavior in primates: A review of evidence and theory

Homosexual behavior is defined as genital contact, genital manipulation or both between same-sex individuals. Available data indicate that this behavior is phylogenetically widespread among the anthropoid primates, but totally absent among prosimians. The majority of the 33 species that demonstrate homosexual behavior do so rarefy, but for a substantial number (N =12) it appears to be a more common pattern under free-ranging conditions. I summarize data on homosexual behavior as it relates to form, living condition, age, sex, social organization, and ecological context, and discuss hormonal, demographic, and sociosexual theories for primate homosexual behavior. Among adult primates, the behavior is not the product of abnormal excesses or deficiencies in androgens. Prenatal excesses of androgens may have some effect on the expression of female homosexual behavior, but these effects might vary over the life span, and data are equivocal at present. Demographic processes that result in skewed sex ratios can favor the expression of homosexual behavior in a population, which causes intraspecific variation. I examine several sociosexual explanations, including (a) proceptivity enhancement, (b) receptivity reduction, (c) dominance assertion, (d) practice for heterosexual copulation, (e) tension regulation, (f) reconciliation, and (g) alliance formation. An evolutionary scenario highlights the transformations this behavior underwent during the evolution of the anthropoid primates. I suggest exaptation as a theoretical framework for interpreting homosexual behavior and conclude that future consideration of sexual selection among primates should address homosexual components of this process.     

Homosexual behavior in wild Sumatran orangutans (Pongo pygmaeus abelii).

Wild male Sumatran orangutans at two study sites engaged in homosexual behavior. These observations demonstrate that homosexual behavior is not an artifact of captivity or contact with humans. In separate instances, homosexual behavior was associated with affiliative and agonistic behaviors. These observations add orangutans to the list of primates in which homosexual behavior forms part of the natural repertoire of sexual or sociosexual behavior.     

Sleep and nesting behavior in primates: A review

Sleep is a universal behavior in vertebrate and invertebrate animals, suggesting it originated in the very first life forms. Given the vital function of sleep, sleeping patterns and sleep architecture follow dynamic and adaptive processes reflecting trade-offs to different selective pressures. Here, we review responses in sleep and sleep-related behavior to environmental constraints across primate species, focusing on the role of great ape nest building in hominid evolution. We summarize and synthesize major hypotheses explaining the proximate and ultimate functions of great ape nest building across all species and subspecies; we draw on 46 original studies published between 2000 and 2017. In addition, we integrate the most recent data brought together by researchers from a complementary range of disciplines in the frame of the symposium “Burning the midnight oil” held at the 26th Congress of the International Primatological Society, Chicago, August 2016, as well as some additional contributors, each of which is included as a “stand-alone” article in this “Primate Sleep” symposium set. In doing so, we present crucial factors to be considered in describing scenarios of human sleep evolution: (a) the implications of nest construction for sleep quality and cognition; (b) the tree-to-ground transition in early hominids; (c) the peculiarities of human sleep. We propose bridging disciplines such as neurobiology, endocrinology, medicine, and evolutionary ecology, so that future research may disentangle the major functions of sleep in human and nonhuman primates, namely its role in energy allocation, health, and cognition.     

Effects of Environmental and Social Conditions on Homosexual Pairing in the Japanese Beetle (Popillia japonica Newman)

Homosexual pairing between males occurs under natural conditions in a wide variety of taxa, including many insect species, but few studies have investigated how environmental and social conditions affect same-sex pairing in insects. We investigated factors affecting homosexual pairing in male Japanese beetles (Popillia japonica Newman) in the field and in the laboratory. Specifically, we investigated how time of day, sex ratio, beetle density, and temperature affected the likelihood of homosexual pairing. In the field, male–male pairs constituted 1–6% of the pairs we collected. Homosexual pairs were more common in the afternoon than in the morning and the evening. Sex ratio, density, and temperature were all related to the likelihood of finding a homosexual pair, but the relationships were not linear. In the laboratory, higher male densities and relatively male-biased sex ratios were associated with an increase in the frequency of homosexual pairs. Homosexual pairs were more frequent at relatively low and relatively high temperatures. Males that mounted other males tended to be smaller than the males that they mounted. In addition, compared to males that were not homosexually paired, there was some indication that the mounting males were smaller, and the mounted males larger, than the unpaired males. Our data suggest that homosexual pairs are a result of males mistaking other males for females, and we hypothesize that the environmental and social factors cause changes in homosexual pairing through their effects on the frequency of pair formation and pair duration.     

Mountain gorilla life histories,reproductive competition,and sociosexual behavior and some implications for captive husbandry

New data on modal patterns of, and variability in, mountain gorilla life history tactics and sociosexual behavior, collected during long-term fieldwork at the Karisoke Research Centre, are presented here. These data show that immature males and females develop sociosexual relationships with both peers and adults, and that these relationships—which contribute to more complex social relationships—often lead to mating between natal females and males who are “familiar” partners. They also show that within-group reproductive competition between males can reach considerable levels, but that immature males are sometimes able to copulate with both nulliparous and parous females; that unrelated silverbacked males can reside in the same all-male group but become intolerant of each other if females join the group; and that, whereas females sometimes compete with each other for opportunities of copulate, their probability of conceiving is probably not decreased by any inability to control the mating situation. This information may contribute to continued improvement in the husbandry of captive gorillas.     

Chimpanzee genital swelling and its role in the pattern of sociosexual behavior

Behavioral observations were made on thirteen female and seven male adult group-living chimpanzees (Pan troglodytes). The behavioral data were analyzed as a function of the day of the females' menstrual cycles to explore the possible interrelationship between genital swelling and sociosexual behavior of female chimpanzees. Copulatory behavior was confined almost entirely to the period of genital swelling and the occurrence of male-to-female genital inspection (both female- and male-initiated) was negatively correlated with the days from swelling onset, i.e., as the presumed day of ovulation approached, genital inspection decreased, while copulatory behavior increased. In addition, more females groomed their male cagemates during the luteal phase than in the follicular phase of their cycles, whereas male-to-female grooming was positively correlated with the progress of the cycle, with peaks during the time of swelling onset and menstruation. The profile of sociosexual behavior observed throughout the menstrual cycle suggested that, although chimpanzees exhibit an extended period of sexual receptivity and genital swelling, the presumed fertile period is not concealed. The role of genital swelling in chimpanzees is discussed in relation to the possible hormonal effect on female sexuality and the evolution of chimpanzee mating strategies. © 1992 Wiley-Liss, Inc.     

Territorial behavior in primates: A review of recent field studies

Primate field studies of the last decade have reported much information of relevance for understanding primate territoriality. This paper reviews some of that material, considering the primate use of home range and core areas, intertroop vocalizations, and the relevance of these concepts for the analysis of territorial behavior. Finally, several reports of field studies of territorial behavior are reviewed. The data reviewed suggests that there are territory-related spacing mechanisms operating in some primate species. However, territorial relations between primate groups are far from universal even among those species which do establish territories; the significance of territoriality will have to be understood as one of a number of ecological adaptations.     

Dominance index: A simple measure of relative dominance status in primates

A simple measure of relative dominance status (cardinal rank) is described which we have termed the dominance index. Like more familiar techniques for assessing rank order, it is based on the direction of aggressive and submissive behaviors between all possible paired combinations of animals in a social group. Using data from five groups of female rhesus monkeys, it reliably produced the same ordinal ranks as fight interaction matrices. There was also good agreement with the cardinal ranks produced by two additional measures of dominance and with those produced by observer ratings. The dominance index can be calculated when fights have not actually occurred and is largely independent of the frequency of agonistic interactions. It has, therefore, wide application and can estimate dominance during brief sampling periods (one hour) and also in stable groups when agonistic interactions are low. Its application is described in experiments in which the male in a group of females was changed and the hormonal status of the females was altered. Estrogen increased female dominance status relative to other females.     

Baculum length and copulatory behavior in primates

The length of the baculum (os penis) was measured in 74 adult males representing 46 primate species. These data, and a review of previously published measurements, indicate that variation in baculum length among primates is related to taxonomic and behavioral differences. Thus, many New World monkeys have shorter bacula, relative to body weight, than Old World monkeys. The baculum is shorter in colobine monkeys than in cercopithecines. Among the great apes, reduction of the baculum is more pronounced in Pan and Gorilla than in Pongo. Very long bacula are found in some nocturnal prosimians (eg, Lorisidae) and also in Macaca arctoides. A comparison of baculum length relative to body weight was made in 34 species for which detailed information on copulatory behavi or was available. The presence of an elongated baculum was shown to correlate with copulatory patterns involving prolonged intromission and/or the maintenance of intromission during the postejaculatory interval (eg, Galago crassicaudatus, Loris tardigradus, M, arctoides). The evolutionary significance of these observations is discussed and it is suggeted that similar copulatory patterns may occur in species with elongated bacula (eg, Daubentonia, Perodicticus) for which behavioral data are lacking at present. The same hypothesis also applies to an extinct adapid primate which possessed a very large baculum.     

Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: Role of sensory function and age

Male-male courtship behavior was recently reported to be induced in large populations of Drosophila (e.g., 600–1500 flies) by ectopic expression of the white (w) gene. Little is known about the basis of this behavior; in male-female courtship, sensory cues are believed to play an important role. Previous data are consistent with the possibility that misexpression of w causes abnormal reception or processing of sensory information. We show here that w-induced male-male courtship occurs in isolated pairs of flies. Thus the behavior does not depend on sensory cues found only among large populations of flies, or on cues produced only by a small subset of such populations. This finding enabled quantitative analysis of mechanisms that underlie the behavior. Specifically, male-male courtship does not depend on the reception of olfactory information, nor on the reception or generation of auditory cues, as determined by surgical ablation of antennae, maxillary palps, or wings. Although the rapid onset of the behavior following w induction suggested that its basis could lie in a modulation of sensory physiology, we found visual, olfactory, and gustatory function to be normal in physiological or behavioral tests. The only sensory deprivation to produce an effect on male-male courtship was testing under dim red light; the percentage of flies courting another male was reduced to one-fourth of control values. A striking age dependence of the behavior is also documented: courtship between paired male mini-w⁺ flies was not observed in tests of very young (1-day-old) flies, but occurs at high levels between the ages of 1 and 4 weeks. © 1996 John Wiley & Sons, Inc.     

昆虫同性性行为的研究进展

从自然选择和性选择角度分析,同性性行为的存在是一个进化悖论,其成因和意义是当今进化生物学研究的重要科学问题。本文综述了昆虫同性性行为的发生、进化意义和遗传基础等方面的研究进展,分析了研究中存在的问题,并展望了未来的研究方向,以期为昆虫同性性行为的进一步研究提供参考。同时,希望本文能引起更多科学工作者关注昆虫同性性行为,并积极投身到此项研究中来,为该研究领域的发展做出贡献。     

The effects of infant births on the sociosexual behavior and hormonal patterns of a cooperatively breeding primate (Cebuella pygmaea)

This study examined changes in the behavioral and hormonal patterns of cooperatively breeding pairs in a primate species with the passing of time and with specific reproductive events. We (1) compared patterns of sexual, agonistic, and affiliative behavior of newly paired pygmy marmosets with the same behavioral patterns immediately after the birth of their first set of infants; (2) determined if postpartum behavioral differences existed between pairs whose infants lived and those whose infants died; and (3) examined whether behavioral patterns changed over the course of ovarian cycles in parous pygmy marmosets as had been documented in nulliparous pairs. The behavior of pairs was recorded during daily half-hour focal samples for 60 days after pairing, and 30 or 60 days after the birth of infants for pairs whose litters died or lived, respectively. Daily urine samples from females during the study were analyzed for luteinizing hormone and pregnanediol glucuronide concentrations to determine dates of ovulation. The results indicated that males consistently altered their sexual behavior and olfactory monitoring of mates during periovulatory periods in the females' cycles both postpairing and postpartum, while similar rates of social and sexual behavior were maintained between the conditions. Sexual behavior occurred throughout the females' ovarian cycles. Peaks in sexual behavior during the periovulatory period in nulliparous pairs disappeared after the birth of infants. Pairs whose infants died showed higher rates of sexual behavior than pairs with surviving infants. Social and sexual behavior may function to maintain the relationship both during and outside of ovulation, especially with the loss of infants. © 1996 Wiley-Liss, Inc.     

Homosexual behaviour and its longevity cost in females and males of the seed beetle Acanthoscelides obtectus

The level of homosexual behaviour is evaluated in one laboratory population of seed beetle and derived lines selected to reproduce early (E) or late in life (L), where inadvertent selection for either low or high heterosexual activity has been detected. The magnitudes of homosexual interaction, measured as chasing and mounting individuals of the same sex, are estimated over different age classes. These magnitudes are correlated with previously observed levels and patterns of age‐specific variation of heterosexual activity of both sexes in the E and L experimental lines. The results obtained support the perception error hypothesis proposing that a low degree of sexual discrimination is genetically correlated with high sexual activity. The fitness costs of the same‐sex interactions are tested by assessing their effects on longevity. In both sexes, the longevities of homosexual pairs are reduced relative to individually‐housed virgin beetles in both the E and L lines, although homosexual interactions have a more pronounced effect on male survival than on female survival. Although the results obtained suggest that the longevity cost of homosexual interactions can be substantial, this cost is much smaller than the cost of heterosexual interactions.     

Allometry and ecology of feeding behavior and digestive capacity in herbivores: A review

The purpose of this review is to give some perspective of the factors that influence feeding behaviors and the ability of herbivores to adapt to diets. The most important of these are digestibility, ability to select feed, and achievement of a nutritionally adequate intake. Plant morphology, observed feeding behavior, body size, and gut architecture and size impinge upon these factors. Feeding behavior and dietary specializations are associated with adaptations of gut and mouth parts as well as body size. Parallel and overlapping behaviors occur among herbivores and particularly between ruminants and nonruminants. The conventional classifications of grazers, browsers, and selective feeders are blurred by these evolutionary developments. © 1996 Wiley-Liss, Inc.     

Some observations on the sociosexual behavior of a captive male Yangtze finless porpoise calf (Neophocaena phocaenoides asiaeorientalis)

Sociosexual behavior in a captive male Yangtze finless porpoise calf (Neophocaena phocaenoides asiaeorientalis) was studied during its first year postpartum. This behavior was first observed at 1 month postpartum. During the year, (1) each event of the sociosexual behavior typically lasted 6–9 s and the frequency was 2.8 occurrences h^?1; (2) ventral–ventral was the predominant sociosexual gesture; (3) prior to sociosexual interactions, the calf generally bonded with the receiver; (4) the mother was his preferred sociosexual partner but other adults of both sexes were also involved; (5) the frequency of sociosexual behavior decreased until the 9th month postpartum and increased thereafter.     

Pair-bond formation and breeding success in the common marmosetCallithrix jacchus jacchus

The breeding records from 22Callithrix jacchus jacchus females aged 13–23 months were examined. It was evident that females aged more than 18 months when first paired bred sooner, as did females paired with sexually experienced males. A detailed behavioral investigation of nine newly formed pairs was carried out for 10 weeks. Males showed more following, sniffing, tail-raised presents, and affectional behavior than their mates, while females showed more soliciting. Only females gave the submissive vocalization (ngÄ). This shows that there is a degree of sexual dimorphism in the behavior of this monogamous monkey. Four of the nine pairs failed to conceive within 12 weeks of pairing;the females of these pairs behaved more submissively than successful breeders, showing more ngÄ and less bristling and sexual behavior. In all cases the four females were housed in close proximity to dominant relatives and this was considered to be a significant factor.     

Same-sex sexual behavior in birds: expression is related to social mating system and state of development at hatching

We report the findings of a phylogenetic comparative analysisexamining patterns and frequency of occurrence of same-sex courtshipand mounting behavior in birds. Our analysis has shown associationsbetween same-sex sexual behavior and both mating system anddegree of precociousness at hatching. The patterns of expressionand frequency of occurrence of same-sex sexual behavior differedmarkedly for males and females. Patterns of same-sex sexualexpression reflected the competitive sexes that actively solicitsexual interactions in heterosexual encounters. Male–male(MM) sexual behavior occurred across all mating systems, butMM mounting was significantly more prevalent in those specieswith facultative polygamy. The frequency of MM sexual behaviorincreased with degree of polygamy. Female–female (FF)sexual behavior (especially courtship) occurred most frequentlyin socially monogamous species and rarely occurred in speciesthat display obligate polygamy (predominantly polygynous species).Both expression and frequency of FF sexual behavior was stronglyrelated to the precocial state of development at hatching. FFsexual behavior is more likely to occur in species in whichmonogamy occurs together with the production of precocial offspring;that is, in monogamous species that are exceptions to the morecommon altricial mode of development. We suggest that requirementof biparental care in monogamous species may influence the greaterexpression of FF sexual behavior and longer term associations.Both spatial and behavioral dispersion of females and engagementin uniparental care may be important in explaining the lowerincidence of FF sexual behavior in polygynous species. Socialcontexts where males congregate at communal leks or displayareas may influence the greater expression and frequency ofMM sexual behavior in polygynous species.