Dispersal Patterns of Orang-utans (<Emphasis Type="BoldItalic">Pongo</Emphasis> spp.) in a Bornean Peat-swamp Forest

Knowledge regarding dispersal patterns in great apes may help in understanding the evolution of dispersal patterns and social grouping in early hominoids, as well as in our own species. However, the social structure and dispersal system of orang-utans (Pongo spp.) remains little understood despite past research. We addressed this question by conducting genetic analyses on a wild orang-utan (Pongo pygmaeus wurmbii) population from the Sabangau peat-swamp in Borneo. We estimated pairwise relatedness among 16 adult individuals using 19 polymorphic microsatellite markers. Mean relatedness among females was significantly higher than in males, irrespective of the relatedness estimator used, following the pattern predicted for male dispersal. Our results support field observations that average dispersal distance for females is less than for males, suggesting that female orang-utans are philopatric, whereas males disperse. This contrasts with previous findings from other sites where anthropogenic influences were present. Based on qualitative mitochondrial DNA analyses, it appears that unflanged adult males show some degree of site fidelity compared to flanged males. Thus, male orang-utans may disperse permanently from their natal range once they are fully flanged. Male-biased dispersal and female philopatry in orang-utans differ from those of extant African apes and are more similar to many Old World monkey species. Hence we hypothesize that this system may represent the ancestral state of early hominoids.     

Reproductive success of two male morphs in a free-ranging population of Bornean orangutans

The reproductive success of male primates is not always associated with dominance status. For example, even though male orangutans exhibit intra-sexual dimorphism and clear dominance relationships exist among males, previous studies have reported that both morphs are able to sire offspring. The present study aimed to compare the reproductive success of two male morphs, and to determine whether unflanged males sired offspring in a free-ranging population of Bornean orangutans, using 12 microsatellite loci to determine the paternity of eight infants. A single flanged male sired most of the offspring from parous females, and an unflanged male sired a firstborn. This is consistent with our observation that the dominant flanged male showed little interest in nulliparous females, whereas the unflanged males frequently mated with them. This suggests that the dominant flanged male monopolizes the fertilization of parous females and that unflanged males take advantage of any mating opportunities that arise in the absence of the flanged male, even though the conception probability of nulliparous females is relatively low.     

The response of adult orang-utans to flanged male long calls: inferences about their function

Flanged male orang-utans emit loud vocalizations called long calls. In this study, we examined the correlates of variation in long-calling rates among flanged male Sumatran orang-utans, as well as the ranging responses of adult females and flanged males to these long calls. Males that gave calls more often were more likely to approach calls by others. Results bolster a female attraction function of long calls. Flanged males did not significantly avoid or approach long calls. However, males called more when alone than when guarding a female mate, and adult females significantly approached long calls, especially those of the dominant male, and did so regardless of their reproductive state, allowing them to remain within earshot of calling males. The possible selective advantages of this response include avoidance of harassment and infanticide by males. These findings confirm the existence of some form of social organization above the mother-infant unit.     

The orang-utan mating system and the unflanged male: A product of increased food stress during the late Miocene and Pliocene?

The orang-utan is unique among apes in having an unusually long male developmental period and two distinct adult male morphs (flanged and unflanged), which generally, but not exclusively, employ different reproductive strategies (call-and-wait vs. sneak-and-rape). Both morphs have recently been shown to have roughly similar levels of reproductive success in the one site where such a study has been conducted. This is in stark contrast to the unimale polygynous gorilla, in which dominant males sire almost all infants. Despite this, evidence on sexual dimorphism, life history, diet, and socioecology of extant and extinct apes, as well as the ontogeny, reproductive morphology, and physiology of extant apes, all indicate that the orang-utan's present-day mating system most likely evolved from a gorilla-like base, with one dominant male guarding a harem of females. The available evidence indicates that, due chiefly to the likely onset of the El Ni?o Southern Oscillation (generally regarded as the trigger for mast fruiting in dipterocarps) approximately 3-5Ma, southeast Asian forests would have begun to experience longer and more severe periods of low food availability. This change in food availability would have meant that full-time gregariousness was no longer energetically tolerable and, as a result, females dispersed more widely in search of food and adult/flanged males were no longer able to effectively guard a harem of females. A niche for a quiet, quick, opportunistic "sexual predator" (i.e., the unflanged male) then became available. This finding implies that, despite being anatomically quite chimpanzee-like, the ancestral hominoid probably had a social and mating system more similar to the gorilla than any other living ape.     

Philopatry and reproductive success in Bornean orang-utans (Pongo pygmaeus)

Behavioural observations suggest that orang-utans are semi-solitary animals with females being philopatric and males roaming more widely in search of receptive partners, leading to the prediction that females are more closely related than males at any given site. In contrast, our study presents evidence for male and female philopatry in the orang-utan. We examined patterns of relatedness and parentage in a wild orang-utan population in Borneo using noninvasively collected DNA samples from animals observed to defecate, and microsatellite markers to assess dispersal and mating strategies. Surprisingly, resident females were equally as related to other resident females (mean r(xy) = 0.303) as resident males were to other resident males (mean r(xy) = 0.305). Moreover, resident females were more related to each other and to the resident males than they were to nonresident females, and resident males were more related to each other (and resident females) than they were to nonresident males. We assigned genetic mothers to 12 individuals in the population, while sires could be identified for eight. Both flanged males and unflanged males achieved paternity, similar to findings reported for Sumatran orang-utans.     

Reproductive strategies of the orang-utan: New data and a reconsideration of existing sociosexual models

Recent field data indicate that MacKinnon’s model of the orang-utan’s sexual and agonistic activity needs to be revised. In this model, male reproductive activity is concentrated in an extended phase of subadulthood and in early adulthood. According to this model, the role of older adult males is primarily that of range guardian, and in that role they would ensure that the offspring they had generated earlier would have safe access to food resources. This study presents cases suggesting that subadult males, even though sexually active, may have low reproductive success. In previous studies adult males were shown to display less sexual initiative than subadult males. In this study an adult male was at times involved infrequent mating activity in response to proceptive activity of females in the course of consortship. This adult male proved to be a successful breeder, thus refuting the hypothesis of adult male sterility. The female is most likely to conceive through cooperative mating in lengthy consortships with the dominant resident adult male. We hypothesize that the extended subadult phase represents a submissive strategy, allowing subadult males to remain in the home range of adult males but with minimal reproductive success.     

A model for the evolution of developmental arrest in male orangutans

Male Sumatran orangutans (Pongo abelii) may delay for many years the acquisition of the full array of secondary sexual traits, including their characteristic cheek flanges. Such flexible developmental arrest is unique among male primates. Among male Bornean orangutans (Pongo pygmaeus) such long delays appear less common. Here, we develop a simple model to identify the conditions under which developmental arrest can be adaptive. We show that the baseline strategy (i.e., males are not susceptible to arrest) cannot be invaded by the flexible strategy (i.e., males can arrest their development when the conditions are unfavorable) when the potential for high‐ranking unflanged or flanged males to monopolize sexual access to females is low. In contrast, at high monopolization potential, the flexible strategy is the evolutionarily stable strategy. We also derive the proportion of flanged males in the population for each combination of monopolization values. This model concurs with field data that found a different monopolization potential between Bornean and Sumatran flanged males and a lower proportion of flanged males in the population in Sumatran orangutans. Pronounced developmental arrest is linked to very low adult mortality, which explains why it is so limited in its taxonomic distribution. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

The social organisation of a population of Sumatran orang-utans

Female orang-utans in a Sumatran swamp forest live in large, but stable, and widely overlapping home ranges. They preferentially associate with some of their female neighbours, possibly relatives, to form socially distinct clusters that also experience reproductive synchrony. Sexually mature males range more widely than females, but among them the dominant adult male has a relatively more limited range. His ranging and that of the subadult males reflect the local abundance of sexually attractive females. The other adult males tend to avoid these concentrations and focus on areas away from the dominant male. Females show philopatric tendencies. Male-biased sex ratios at birth give way to heavily female-biased sex ratios among adults. This suggests a net loss of males as they mature, due either to excess male mortality (e.g. by male mating competition), excess male dispersal from the population or a combination of both. We conclude that the orang-utan social organisation is best described as a loose community, showing neither spatial nor social exclusivity, consisting of one or more female clusters and the adult male they all prefer as mate.     

Male-Biased Sex Ratios in Offspring of Attractive Males in the Guppy

The attractiveness hypothesis predicts that females produce offspring with male-biased sex ratios when they mate with attractive males because their male offspring will inherit the paternal sexual attractiveness and may have high reproductive success. In this study, we examined the effect of the attractiveness of the male guppy Poecilia reticulata in terms of the conspicuousness of its orange spot patterns, important criteria affecting female choice in this species, on the offspring sex ratios. We found that food-manipulation treatment altered the conspicuousness of the orange spot patterns in a full-sibling male pair. When females were presented to these males, they showed a greater mate preference for males having brighter orange spots than for those having duller orange spots. Subsequently, half of the females were mated with the preferred males and the remaining females were mated with the less preferred males. When the females exhibited a greater preference for their mates, their offspring sex ratios were more male biased. These results appear to be consistent with the prediction of the attractiveness hypothesis. In the guppy, as male sexual attractiveness is heritable, the male-biased sex ratios of the broods of attractive males may be adaptive.     

Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits

Females may invest more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred partners may be fitter than offspring sired by non-preferred ones. In this study, we tested the differential maternal allocation hypothesis in the freshwater crayfish, Austropotamobius italicus, by means of a pairing experiment aimed at evaluating the effects of specific male traits (body size, chelae size and chelae asymmetry) on female primary reproductive effort. Our results showed that females laid larger but fewer eggs for relatively small-sized, large-clawed males, and smaller but more numerous eggs for relatively large-sized, small-clawed males. Chelae asymmetry had no effects on female reproductive investment. While the ultimate consequences of this pattern of female allocation remain unclear, females were nevertheless able to adjust their primary reproductive effort in relation to mate characteristics in a species where inter-male competition and sexual coercion may mask or obscure their sexual preferences. In addition, our results suggest that female allocation may differentially affect male characters, thus promoting a trade-off between the expression of different male traits.     

Predicting the Vulnerability of Great Apes to Disease: The Role of Superspreaders and Their Potential Vaccination

Disease is a major concern for the conservation of great apes, and one that is likely to become increasingly relevant as deforestation and the rise of ecotourism bring humans and apes into ever closer proximity. Consequently, it is imperative that preventative measures are explored to ensure that future epidemics do not wipe out the remaining populations of these animals. In this paper, social network analysis was used to investigate vulnerability to disease in a population of wild orang-utans and a community of wild chimpanzees. Potential ‘superspreaders’ of disease - individuals with disproportionately central positions in the community or population - were identified, and the efficacy of vaccinating these individuals assessed using simulations. Three resident female orang-utans were identified as potential superspreaders, and females and unflanged males were predicted to be more influential in disease spread than flanged males. By contrast, no superspreaders were identified in the chimpanzee network, although males were significantly more central than females. In both species, simulating the vaccination of the most central individuals in the network caused a greater reduction in potential disease pathways than removing random individuals, but this effect was considerably more pronounced for orang-utans. This suggests that targeted vaccinations would have a greater impact on reducing disease spread among orang-utans than chimpanzees. Overall, these results have important implications for orang-utan and chimpanzee conservation and highlight the role that certain individuals may play in the spread of disease and its prevention by vaccination.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

Female reproductive strategies in orangutans,evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion

Intersexual conflicts over mating can engender antagonistic coevolution of strategies, such as coercion by males and selective resistance by females. Orangutans are exceptional among mammals for their high levels of forced copulation. This has typically been viewed as an alternative mating tactic used by the competitively disadvantaged unflanged male morph, with little understanding of how female strategies may have shaped and responded to this behaviour. Here, we show that male morph is not by itself a good predictor of mating dynamics in wild Bornean orangutans but that female conception risk mediated the occurrence and quality of male–female interactions. Near ovulation, females mated cooperatively only with prime flanged males who they encountered at higher rates. When conception risk was low, willingness to associate and mate with non-prime males increased. Our results support the hypothesis that, together with concealed ovulation, facultative association is a mechanism of female choice in a species in which females can rarely avoid coercive mating attempts. Female resistance, which reduced copulation time, may provide an additional mechanism for mate selection. However, coercive factors were also important as prime males were frequently aggressive to females and females used mating strategies consistent with infanticide avoidance.     

Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis

Various hypotheses have been proposed to account for the functionof sexual swellings in female primates, but few empirical dataexist to test predictions arising from these hypotheses. Controversyhas recently arisen over a field study that appeared to supportthe predictions of the reliable indicator hypothesis. This hypothesisproposes that females compete for males or matings, that differencesin swelling size between females reliably advertise female quality,and that males use swelling characteristics to differentiallyallocate mating effort to females with certain swelling characteristics,hence to females of higher quality. To provide an independenttest of this hypothesis, we collected data concerning the sizeand coloration of 40 sexual swellings for 29 semi-free-rangingfemale mandrills, varying in age and parity, along with dataconcerning the behavior of males toward the females, and comparedthese with the long-term reproductive history of the females.We examined the following predictions: (1) swelling characteristicsare consistent across subsequent cycles for individual females,(2) swelling characteristics indicate aspects of female reproductivequality, and (3) males prefer to mate with females that showparticular swelling characteristics. Our results support prediction1; we found little change in swelling characteristics acrossswellings for individual females. However, we found no significantrelationships between female reproductive history and swellingcharacteristics and, thus, no support for prediction 2. Finally,we found only limited support for prediction 3; females withlarger (wider) sexual swellings were more likely to have a spermplug when maximally swollen. However, male mate-guarding wasnot significantly related to female swelling characteristics.Furthermore, in situations in which more than one female wasmaximally swollen, the alpha male (who has "free" choice) didnot show the most interest in the female with the largest swelling.We conclude that the reliable indicator hypothesis does notexplain variation in sexual swellings in female mandrills.     

Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure

Mammalian play is believed to improve motor skills as well as facilitate the development of social relationships. Given the marked sexual dimorphism in gorilla body size and the role assumed by the male in protecting the group from conspecifics and predators, the motor-training hypothesis of play predicts that male infants should exhibit higher frequencies of social play than female infants, and that males should prefer to play with other males. Given that adult female gorillas are strongly attracted to adult breeding males and form only weak social bonds with unrelated adult females, the social-relationship hypothesis of play predicts that female infants should prefer to play with males. These hypotheses were tested in a 22-month study of 12 gorilla infants, aged between 0-5 years, living in three zoological parks in Chicago and Atlanta. Consistent with the hypotheses, male infants played more than female infants did, and both male and female infants preferred to play with males rather than with females. These findings suggest that sex differences in play in the great apes and other primates can be predicted by the characteristics of adult behavior and social structure above and beyond the patterns of sex-biased dispersal or coalition formation with same-sex kin.     

Sex differences in biparental care as offspring develop: a field study of convict cichlids (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

Parental investment theory states that parents should contribute more to older offspring. Differences between the sexes also influence how each parent contributes to offspring in biparental species. Here, we examined a naturally occurring population of biparental convict cichlids in Costa Rica to determine how each parent cared for offspring during two distinct offspring development stages. Consistent with the predictions of the reproductive value hypothesis, we hypothesized that the levels of parental contribution would be relative to the value that each parent places on a brood. We predicted that female parents would contribute more than male parents because female convict cichlids have lower future reproductive success than males. Additionally, we predicted that both parents should contribute more to older offspring, either due to the young’s increased susceptibility to predation (i.e., the vulnerability hypothesis) or because of the longer period of time parents have been interacting with older offspring (i.e., feedback hypotheses). This increase in investment by males should coincide with a change in the coordination of care between parents. Detailed observations of parental pairs in their natural habitat supported these predictions. Females contributed more to broods than males and were relatively unaffected by offspring age while males spent significantly more time with older, free-swimming fry. Additionally, males tended to leave younger offspring more than females did, and were more likely to do so consecutively with younger offspring. This suggests that the coordination of duties between parents changes as parental investment changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not necessarily the feedback hypothesis.     

Sexual segregation in childhood: a review of evidence for two hypotheses

In this paper, I review the evidence associated with two hypotheses, both ultimately derived from sexual selection theory, put forth to explain social sexual segregation in human juveniles. More proximately, I posit that segregation is motivated by sex differences in body size, physical activity and competitiveness. The first hypothesis, the energetic/behavioural hypothesis, suggests that difference in energetics is a way in which males differentiate themselves from females and develop muscle and brain systems implicated in reproductive roles. The second hypothesis, the social roles hypothesis, suggests that segregation is related to learning male and female reproductive roles. The reviewed evidence supports the view that there are differences in energetics in male and female groups. With development, the vigorous behaviours shown by males take the form of specific social roles, related to dominance and competitiveness for males and maternal roles for females.     

Costs of rearing and sex‐ratio variation in southern grey shrike Lanius meridionalis broods

Several non‐mutually exclusive hypotheses predict adaptive variation in the offspring sex ratio. When conditions for breeding are adverse, parents are predicted to produce more offspring of the less costly sex to rear (‘the cost‐of‐reproduction hypothesis’). Moreover, they also should produce the more dispersing sex in order to diminish future competition (‘the local‐resource‐competition hypothesis’). Here, we analyse brood sex ratio according to rearing conditions in the southern shrike Lanius meridionalis, a species with moderately reversed sexual dimorphism. Our results suggest that females are more costly to rear than males in this species. Adult females proved heavier than males, and female nestling tended to be heavier than male nestlings. Moreover, the greater brood reduction, the more male‐biased was the brood, suggesting that brood reduction implied higher mortality in female nestlings. Consistent with these findings, the brood sex ratio was biased to the less costly sex (males) when breeding conditions were adverse (bad years or low‐quality male parents), supporting the cost‐of‐reproduction hypothesis. By contrast, these findings did not support the local‐resource‐competition hypothesis, which predicted female‐biased brood sex ratio under adverse conditions. As a whole, our results support the idea that birds adaptively modulate sex ratio in order to minimize reproduction costs.     

Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication

Orangutans display remarkable developmental changes and sexual differences in facial morphology, such as the flanges or cheek-pads that develop only on the face of dominant adult males. These changes suggest that facial morphology is an important factor in visual communication. However, developmental changes in facial morphology have not been examined in detail. We studied developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus) by observing 79 individuals of various ages living in the Sepilok Orangutan Rehabilitation Centre (SORC) in Malaysia and in Japanese zoos. We also analyzed photographs of one captive male that were taken over a period of more than 16 years. There were clear morphological changes that occurred with growth, and we identified previously unreported sexual and developmental differences in facial morphology. Light-colored skin around the eyes and mouth is most prominent in animals younger than 3 years, and rapidly decreases in area through the age of approximately 7 years. At the same time, the scattered, erect hairs on the head (infant hair) become thick, dense hairs lying on the head (adult hair) in both sexes. The results suggest that these features are infant signals, and that adult signals may include darkened face color, adult hair, whiskers, and a beard, which begin to develop after the age of approximately 7 years in both sexes. In females, the eyelids remain white even after 10 years, and turn black at around the age of 20; in males, the eyelids turn black before the age of 10. The whiskers and beards of adults are thicker in males than in females, and are fully developed before the age of 10 in males, while they begin to develop in females only after approximately 20 years. White eyelids and undeveloped whiskers and beards may be visual signals that are indicative of young adult females. Our results also show that the facial morphology of the unflanged male is similar to that of the adult female, although it has also been pointed out that unflanged males resemble younger individuals.