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.     

The accelerated evolution of human cytochrome c oxidase – Selection for reduced rate and proton pumping efficiency?

The cytochrome c oxidase complex, complex VI (CIV), catalyzes the terminal step of the mitochondrial electron transport chain where the reduction of oxygen to water by cytochrome c is coupled to the generation of a protonmotive force that drive the synthesis of ATP. CIV evolution was greatly accelerated in humans and other anthropoid primates and appears to be driven by adaptive selection. However, it is not known if there are significant functional differences between the anthropoid primates CIV, and other mammals. Comparison of the high-resolution structures of bovine CIV, mouse CIV and human CIV shows structural differences that are associated with anthropoid-specific substitutions. Here I examine the possible effects of these substitutions in four CIV peptides that are known to affect proton pumping: the mtDNA-coded subunits I, II and III, and the nuclear-encoded subunit VIa2. I conclude that many of the anthropoid-specific substitutions could be expected to modulate the rate and/or the efficiency of proton pumping. These results are compatible with the previously proposed hypothesis that the accelerated evolution of CIV in anthropoid primates is driven by selection pressure to lower the mitochondrial protonmotive force and thus decrease the rate of superoxide generation by mitochondria.     

Homosexual Fellatio: Erect Penis Licking between Male Bonin Flying Foxes Pteropus pselaphon

A recent focus of interest has been on the functional significance of genital licking (fellatio and cunnilingus) in relation to sexual selection in Pteropodid bats. In the present paper, a form of fellatio in wild Bonin flying foxes, Pteropus pselaphon, performed between adult males has been reported. During the mating season, adult flying foxes roost in same-sex groups, forming ball-shaped clusters which provide warmth. The female clusters may also contain a few males. Unassociated with allogrooming, same-sex genital licking occurred among males in the all male clusters. As such, male-male fellatio can be considered as homosexual behavior, two functional explanations could account for this behavior; the social bonding and the social tension regulation hypotheses suggested in a previous review. Given that neither the simpler alternative that in all male groups such fellatio may represent misdirected sexual behavior, nor the two previously proposed functional hypotheses were supported by the data, I propose another functional hypothesis. Homosexual fellatio in this species could help males solve inconsistent situations in the roost when there are conflicts between cooperative behavior for social thermoregulation and competition for mating.     

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.     

Evolution of locomotion in Anthropoidea: the semicircular canal evidence

Our understanding of locomotor evolution in anthropoid primates has been limited to those taxa for which good postcranial fossil material and appropriate modern analogues are available. We report the results of an analysis of semicircular canal size variation in 16 fossil anthropoid species dating from the Late Eocene to the Late Miocene, and use these data to reconstruct evolutionary changes in locomotor adaptations in anthropoid primates over the last 35 Ma. Phylogenetically informed regression analyses of semicircular canal size reveal three important aspects of anthropoid locomotor evolution: (i) the earliest anthropoid primates engaged in relatively slow locomotor behaviours, suggesting that this was the basal anthropoid pattern; (ii) platyrrhines from the Miocene of South America were relatively agile compared with earlier anthropoids; and (iii) while the last common ancestor of cercopithecoids and hominoids likely was relatively slow like earlier stem catarrhines, the results suggest that the basal crown catarrhine may have been a relatively agile animal. The latter scenario would indicate that hominoids of the later Miocene secondarily derived their relatively slow locomotor repertoires.     

Comparative Perspectives on Bimaturism, Ontogeny, and Dimorphism in Lemurid Primates

We address questions regarding the general absence of dimorphism in lemurid primates (Hapalemur, Eulemur, and Varecia) through comparative analyses of ontogeny. We described and analyzed body mass growth data for 9 lemurid taxa and compared them to similar data for anthropoid primates. Lemurids tend to grow rapidly over a short period of time when compared to anthropoid primates of similar body sizes. Size variation among lemurid taxa arises primarily as a consequence of differences in rates of growth. Comparative analyses of body mass growth data suggest that natural selection has produced ontogenetic adaptations in lemurids that center on relatively short periods of growth. Reduced growth periods preclude the evolution of sexual dimorphism through bimaturism—a sex difference in the length of the growth period—despite high levels of intermale competition. Selective factors related to seasonal variability of lemurid habitats play important roles in limiting the potential for the evolution of bimaturism. Other selective factors that limit bimaturism are related to female reproductive synchrony. In combination, they favor relatively early male maturation, precluding sexual selection that would otherwise promote the evolution of dimorphism through bimaturism. Natural selection on growth rates may preclude somatic responses to sexual selection that involve elevated male growth rates. In general, existing ontogenetic or life history adaptations appear to restrict responses to sexual selection in male lemurids.     

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.     

Telomere Biology and Cellular Aging in Nonhuman Primate Cells

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs.     

Evolution of human growth spurts

This study investigates subadult growth spurts in a large sample of anthropoid primates, including humans. Analyses of body mass growth curves show that humans are not unique in the expression of female and male body mass growth spurts. Subadult growth spurts are observed in both New World and Old World anthropoid primates and are more common in males than in females. Allometric analyses of growth spurts indicate that many aspects of primate growth spurts are strongly correlated with species size. Small species tend not to exhibit growth spurts. Although male and female scaling patterns for velocity and size measures are comparable, scaling relations of variables that measure the timing of growth spurts differ by sex. These patterns can he related to sexual differences in life histories. Scaling analyses further show that humans do not depart substantially from patterns that describe other anthropoid primates. Thus, in relative terms, human growth spurts are not exceptional compared to this sample of primates. The long absolute delay in the initiation of the human growth spurt may be of substantial evolutionary importance and serves to distinguish humans from other primates. In essence, humans exhibit growth spurts that are comparable to other primates in many respects. However, human growth spurts are shifted to very late absolute ages. © 1996 Wiley-Liss, Inc.     

Sociosexuality as predictor of sexual harassment and coercion in female and male high school students

Sexual harassment and coercion have mainly been considered from a sex difference perspective. While traditional social science theories have explained harassment as male dominance of females, the evolutionary perspective has suggested that sex differences in the desire for sex are a better explanation. This study attempts to address individual differences associated with harassment from an evolutionary perspective. Considering previous research that has found links between sociosexual orientation inventory (SOI) and harassment, we consider whether this association can be replicated in a large, representative sample of high school students (N=1199) from a highly egalitarian culture. Expanding the previous studies which mainly focused on male perpetrators and female victims, we also examine females and males as both perpetrators and as victims. We believe that unrestricted sociosexuality motivates people to test whether others are interested in short-term sexual relations in ways that sometimes might be defined as harassment. Furthermore, unrestricted individuals signal their sociosexual orientation, and while they do not desire all individuals that react to these signals with sexual advances, they attract much more sexual advances than individuals with restricted sociosexual orientations, especially from other unrestricted members of the opposite sex. This more or less unconscious signaling thus makes them exploitable, i.e., harassable. We find that SOI is a predictor for sexual harassment and coercion among high school students. The paper concludes that, as expected, unrestricted sociosexuality predicts being both a perpetrator and a victim of both same-sex and opposite-sex harassment.     

Differential Responses of Brain,Gonad and Muscle Steroid Levels to Changes in Social Status and Sex in a Sequential and Bidirectional Hermaphroditic Fish

Sex steroids can both modulate and be modulated by behavior, and their actions are mediated by complex interactions among multiple hormone sources and targets. While gonadal steroids delivered via circulation can affect behavior, changes in local brain steroid synthesis also can modulate behavior. The relative steroid load across different tissues and the association of these levels with rates of behavior have not been well studied. The bluebanded goby (Lythrypnus dalli) is a sex changing fish in which social status determines sexual phenotype. We examined changes in steroid levels in brain, gonad and body muscle at either 24 hours or 6 days after social induction of protogynous sex change, and from individuals in stable social groups not undergoing sex change. For each tissue, we measured levels of estradiol (E₂), testosterone (T) and 11-ketotestosterone (KT). Females had more T than males in the gonads, and more E₂ in all tissues but there was no sex difference in KT. For both sexes, E₂ was higher in the gonad than in other tissues while androgens were higher in the brain. During sex change, brain T levels dropped while brain KT increased, and brain E₂ levels did not change. We found a positive relationship between androgens and aggression in the most dominant females but only when the male was removed from the social group. The results demonstrate that steroid levels are responsive to changes in the social environment, and that their concentrations vary in different tissues. Also, we suggest that rapid changes in brain androgen levels might be important in inducing behavioral and/or morphological changes associated with protogynous sex change.     

Scaling of limb joint surface areas in anthropoid primates and other mammals

Recently it was reported that limb joint surface areas scale positively allometrically with body weight in anthropoid primates. This was attributed to the biomechanics of weight bearing: larger animals must require relatively larger joint surfaces to withstand relatively greater weight-related stresses on the joints. Our data on humeral and femoral geometry and joint surface areas in 73 species belonging to six mammalian orders (including primates) demonstrate that positive allometry of joint surface areas is not a general phenomenon for mammals and cannot have its basis among Anthropoidea in the biomechanics of weight bearing. We argue that, to the extent that positive allometric scaling of joint surface areas occurs in anthropoid primates, it is an artifact of differences in positional behaviour among distinct taxonomic groups that also happen to differ widely in body weight. Furthermore, we argue that, among mammals ranging in body size from sportive lemurs to giant pandas, functionally similar groups tend to exhibit: (1) linear dimensions (especially diameters and shaft circumferences) that scale in direct proportion to each other; and (2) joint surface areas that scale in direct proportion to the squares of linear dimensions and to the 2/3 power of body mass. In other words, limb bones of functionally similar animals fit the theoretical model of geometric similarity (or skeletal isometry). Differences in relative sizes of joint surface areas are related to differences in force transmission and movement potential among functionally distinct groups of animals.     

Interaction of bisphenol A (BPA) and soy phytoestrogens on sexually dimorphic sociosexual behaviors in male and female rats

Concerns have been raised regarding the potential for endocrine disrupting compounds (EDCs) to alter brain development and behavior. Developmental exposure to bisphenol A (BPA), a ubiquitous EDC, has been linked to altered sociosexual and mood-related behaviors in various animal models and children but effects are inconsistent across laboratories and animal models creating confusion about potential risk in humans. Exposure to endocrine active diets, such as soy, which is rich in phytoestrogens, may contribute to this variability. Here, we tested the individual and combined effects of low dose oral BPA and soy diet or the individual isoflavone genistein (GEN; administered as the aglycone genistin (GIN)) on rat sociosexual behaviors with the hypothesis that soy would obfuscate any BPA-related effects. Social and activity levels were unchanged by developmental exposure to BPA but soy diet had sex specific effects including suppressed novelty preference, and open field exploration in females. The data presented here reinforce that environmental factors, including anthropogenic chemical exposure and hormone active diets, can shape complex behaviors and even reverse expected sex differences.     

Exceptional longevity and exceptionally high metabolic rates in anthropoid primates are linked to a major modification of the ubiquinone reduction site of cytochrome b

The maximal lifespan of Anthropoid primates (monkeys, apes and humans) exceed the lifespan of most other mammals of equal body mass. Unexpectedly, their exceptional longevity is associated with exceptionally high metabolic rates, in apparent contradiction to the Free Radical Theory of Aging. It was therefore suggested that in anthropoid primates (and several other taxa of mammals and birds) the mitochondrial electron transport complexes evolved to modify the relationship between basal electron transport and superoxide generation to allow for the evolution of exceptional longevity. Cytochrome b, the core protein of the bc1 complex is a major source of superoxide. The amino-acid sequence of cytochrome b evolved much faster in anthropoid than in prosimian primates, and most other mammals, resulting in a large change in the amino-acids composition of the protein. As a result of these changes cytochrome b in anthropoid primates is significantly less hydrophobic and contains more polar residues than other primates and most other mammals. Most of these changes are clustered around the reduction site of uboiquinone. In particular a key positively charged residue, arginine 313, that interacts with propionate D of heme b_H, and thus raises its redox potential, is substituted in anthropoid primates with the neutral residue glutamine, most likely resulting in a lower redox potential of heme b_H and faster reduction of ubiquinone at high proton motive force. It is suggested that these changes contribute to the observed increased rates of basal metabolism and reduce the rates of superoxide production, thus allowing for increased lifespan.     

Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence

Recent fossil discoveries have demonstrated that Africa and Asia were epicentres for the origin and/or early diversification of the major living primate lineages, including both anthropoids (monkeys, apes and humans) and crown strepsirhine primates (lemurs, lorises and galagos). Competing hypotheses favouring either an African or Asian origin for anthropoids rank among the most hotly contested issues in paleoprimatology. The Afrocentric model for anthropoid origins rests heavily on the >45 Myr old fossil Algeripithecus minutus from Algeria, which is widely acknowledged to be one of the oldest known anthropoids. However, the phylogenetic position of Algeripithecus with respect to other primates has been tenuous because of the highly fragmentary fossils that have documented this primate until now. Recently recovered and more nearly complete fossils of Algeripithecus and contemporaneous relatives reveal that they are not anthropoids. New data support the idea that Algeripithecus and its sister genus Azibius are the earliest offshoots of an Afro–Arabian strepsirhine clade that embraces extant toothcombed primates and their fossil relatives. Azibius exhibits anatomical evidence for nocturnality. Algeripithecus has a long, thin and forwardly inclined lower canine alveolus, a feature that is entirely compatible with the long and procumbent lower canine included in the toothcomb of crown strepsirhines. These results strengthen an ancient African origin for crown strepsirhines and, in turn, strongly challenge the role of Africa as the ancestral homeland for anthropoids.     

Patterns of dental emergence in early anthropoid primates from the Fayum Depression,Egypt

Abstract

Paleontological field work in the Fayum Depression of Egypt has produced a remarkable diversity of fossil anthropoids, and this, combined with advances in genetic analyses of living anthropoids, has led to establishment of a temporal and phylogenetic framework for anthropoids that is achieving some degree of consensus. Less well understood are the evolutionary mechanisms and selective factors behind the origin and early diversification of anthropoids. One area that has remained under explored is investigation into the life history patterns of early anthropoids, a major omission given that understanding patterns of growth and development is essential for interpreting the paleobiology of fossil species. Here we detail dental emergence sequences for five species in four families of early anthropoid primates from the Fayum, and use these data to test Schultz’s Rule concerning the timing of emergence of molars versus premolars in mammals. Two important results are generated: (1) only one species had a dental eruption sequence identical to that observed among crown catarrhine primates; and (2) in all cases, the permanent canine was the last post-incisor dental element to fully erupt, a finding that may be significant for interpreting early anthropoid behavioral strategies.