Impact of Male Infanticide on the Social Structure of Mountain Gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.     

Patterns of paternity and group fission in wild multimale mountain gorilla groups

To understand variation among social systems, it is essential to know the relative reproductive success of individuals in group-living species. Particularly interesting for such studies are taxa such as mountain gorillas in which both one-male and multimale groups are common, because of the opportunity to estimate the costs and benefits to males of pursuing different reproductive strategies. We genotyped 68 individuals from two groups of multimale mountain gorilla groups in Bwindi Impenetrable National Park, Uganda to determine the distribution of paternity among the males. In both groups, the dominant male sired the majority of offspring. One group underwent a fission, and we found that the eight offspring assigned to the dominant silverback (and their mothers) remained with their father, while the two offspring of unknown paternity ended up in the small group headed by the formerly subordinate silverback. This is consistent with the proposal that the outcome of group fission in primates is not only influenced by maternal relationships among individuals, but also by patrilineal relationships. Results of this study show that subordinate males may gain reproductive benefits even while queuing for dominance status. Despite ecological differences between Bwindi and the Virunga Volcanoes, male mountain gorillas living in both populations benefit from remaining in multimale groups.     

Mating strategy and reproductive success of male patas monkeys (Erythrocebus patas)

Mating behavior and paternity of offspring of wild patas monkeys were studied at Kala Maloue National Park, Cameroon. Observation of patas groups over three years revealed that multi-male situations occurred after takeover of the position of a resident male. Direct observation of behavior showed that resident males (harem males) occupied only 31% of mating in multi-male situations and 100% in one-male situations. DNA-typing revealed that resident males sired two of four of infants in the one-male situation and four of five in the multi-male situation. Under the two years cycle of the one-male situation and the multi-male situation, calculation shows that resident males sired more offspring than sneakers both in observation and paternity testing. Sneak mating occurred during both one-male and multi-male situations, and resident males performed compensatory mating, with dilution of sneaker sperm; these activities explain the discrepancy found between observation of mating and results of paternity discrimination.     

Male competition and paternity in wild chimpanzees of the Taï forest

In social animals, competition among males for mates affects individual reproductive success. The priority‐of‐access model attempts to account for the influence of demographic conditions within groups upon male reproductive success, but empirical data for testing this model are scarce. Our long‐term study of chimpanzees in the Taï National Park, Côte d'Ivoire, encompasses a period of steady decrease in community size and fluctuating numbers of competing males and sexually receptive females. These demographic changes, in combination with genetic assessment of paternity for 48 offspring from three communities, allowed us to quantify the effects of varying levels of competition upon male reproductive success. On average, the highest‐ranking male sired 50% of all analyzed offspring during a 14‐year period from 1987–2000. Competition among males strongly decreased the relative reproductive success of the alpha male, such that the alpha male's rate of success decreased from 67% with few competitors to only 38% with four or more competitors. The increasing number of synchronously receptive females in large groups also reduced the proportion of paternities by the alpha male. Thus, patterns of paternity in Taï chimpanzees fit well the predictions of the priority‐of‐access model. We also found that despite the inability of dominants to monopolize reproduction, they achieved a higher reproductive rate in large multimale groups, because these have more females and a higher infant survival rate. Varied levels of male competition within communities seem to explain differences in the reproductive success of alpha males observed in different chimpanzee populations, and in other primate species. Am J Phys Anthropol, 2006. © 2005 Wiley‐Liss, Inc.     

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

Variance in the reproductive success of dominant male mountain gorillas

Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.     

Male Competition,Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

Mammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.-Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding-age males and females observed over 4 yr of studying this population.     

Determinants of Paternity Success in a Group of Captive Vervet Monkeys (<Emphasis Type="BoldItalic">Chlorocebus aethiops sabaeus</Emphasis>)

Paternity success of high-ranking primate males is affected by the number of males and the number of fertile females and their cycle synchrony. Female vervets in the wild show strong reproductive seasonality and do not advertise the ovulatory period with conspicuous signals or behavior. Because this makes it difficult for males to monopolize fertile females, it can be expected that male reproductive skew in this species is lower than in other cercopithecines living in multimale groups that advertise the ovulatory period. We assessed male reproductive success in a captive vervet group, initially consisting of 4 males and 12 unrelated females. Besides a general low reproductive skew, we predicted paternity success of the alpha males to be dependent on the overlap of synchronously fertile females, month into alpha male tenure, and housing conditions (the subjects were kept in a large park but had to be locked in a small indoor compartment during the winter months). Further, because the number of males reaching their prime increased over time, we predicted a decrease in reproductive success of the alpha male with increasing tenure length of the alpha male. To assess this we collected genetic samples from 27 of 32 offspring born into the group during 3 yr, using 7 polymorphic human microsatellite markers. Contrary to our predictions, reproductive success of the males occupying the alpha position during the study was among the highest found in cercopithecines, with the alpha males siring 78% of all offspring. The degree of overlapping fertile periods did not affect paternity success, nor did paternity success of the alpha male differ between the 2 housing conditions. Only the alpha male’s tenure length had an effect. Alpha male reproductive success decreased over time, which we attribute to either a shift in female mate choice toward younger males or to increased competition among the males in the later stage of the alpha male’s tenure. This study demonstrates the importance of assessing reproductive success of males throughout >1 season and should spawn more research into the role of female choice and postcopulatory mechanisms in this species.     

Consequences of a One-male Harem Reproductive System and Inbreeding in a Captive Group of <Emphasis Type="BoldItalic">Cercopithecus solatus</Emphasis>

In closed captive populations, where dispersal is not possible, kin recognition and behavioral avoidance are the only mechanisms by which closely related individuals can avoid inbreeding. In the absence of avoidance, a loss of genetic diversity is inevitable in successive generations.In the 1980s, the CIRMF in Gabon established a small breeding group of sun-tailed monkeys (Cercopithecus solatus) with 4 individuals, and subsequently 17 births have been registered. We aimed to describe via microsatellite genotyping the reproductive system in the colony of Cercopithecus solatus, to evaluate the loss of genetic diversity with succeeding generations, and to evaluate consequences of inbreeding depression on a measure of the lifespan reproductive success of females giving birth to inbred vs. noninbred offspring. During the 11-yr period for which data are available, only alpha males sired offspring, confirming a one-male social organization. They reproduced only during their period of tenure. Two of the 3 alpha males were responsible for all the infants born. Genetic diversity decreased and inbreeding coefficients increased with successive generations. Interbirth interval was increased following the birth of an inbred infant, indicating possible increased maternal costs of rearing inbred infants. Loss of genetic variability in this captive group of sun-tailed monkeys has led to significant inbreeding depression and demonstrates the importance of male-mediated gene flow in restricted one-male harem breeding groups.     

Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus)

In the recent past, application of DNA genotyping techniques has enabled researchers to more accurately test relationships between dominance rank (DR), mating success (MS) and reproductive success (RS). Paternity studies often reveal that reproductive outcome does not always correlate with male DR and/or MS and thus open room for discussion and interpretation of alternative reproductive tactics of both sexes. In this study, we analysed male DR, MS and RS in a group of bonobos at Twycross Zoo (UK). Genetic relationships were determined using 8 tetrameric microsatellite loci. Despite clear and asymmetric dominance relationships, analysed using normalised David's scores based on a dyadic index of dominance among the group's 3 mature males, we found that the most dominant male did not sire the most offspring. In fact, both infants conceived during the observation period were found to be sired by the lower-ranking males. Although the alpha male had almost exclusive mating access to one of the females during the time she was showing a maximal anogenital swelling, her infant was sired by the lowest-ranking male who mostly mated with her when outside the maximal swelling period. This result suggests that either sperm competition operates and/or ovulation is decoupled from the phase of maximal anogenital swelling which could allow greater female choice.     

Reproductive success in relation to dominance rank in the absence of prime-age males in Barbary macaques

In some primate species dominance rank of males is correlated with reproductive success, whereas in other species this relationship is inconsistent. Barbary macaques (Macaca sylvanus) live in a promiscuous mating system in which males are ranked in a dominance hierarchy that influences their access to females. High-ranking males usually monopolize fertile females during their estrous period and show increased mating activities. Subadult males generally rank below adult males. For Barbary macaque females in the Gibraltar colony, there was no correlation between dominance status and reproductive success. Paternity data for 31 offspring collected over four consecutive breeding seasons were used to test whether male social rank was associated with reproductive success and whether reproductive success was mainly confined to a small number of males. Genetic variation was assessed using 14 microsatellite markers for a dataset of 127 individuals sampled in all five social groups of the Gibraltar colony. Paternity analysis was conducted for offspring in one social group only, where all in-group males were sampled. Eighty-three percent of the offspring could be assigned to an in-group candidate father; none of the extra-group males appeared to have sired an infant. Male dominance rank was not found to contribute to the observed variation in male reproductive output. Fifty-nine percent of the offspring was sired by two low-ranking males, whereas the two top-ranking males sired one-fifth. A highly significant correlation was found for male age and dominance rank. Reproductive success of subadult males might be explained by the gap in the age distribution of male group members. These missing prime males are usually regarded as serious competitors for older males. Subadult males may have gained easier access to females in their absence. In addition, the presence of inbreeding avoidance mechanisms, which might also have overpowered possible rank effects, cannot be excluded.     

Social bonds enhance reproductive success in male macaques

For animals living in mixed-sex social groups, females who form strong social bonds with other females live longer and have higher offspring survival [1-3]. These bonds are highly nepotistic, but sometimes strong bonds may also occur between unrelated females if kin are rare [2, 3] and even among postdispersal unrelated females in chimpanzees and horses [4, 5]. Because of fundamental differences between the resources that limit reproductive success in females (food and safety) and males (fertilizations), it has been predicted that bonding among males should be rare and found only for kin and among philopatric males [6] like chimpanzees [7-9]. We studied social bonds among dispersing male Assamese macaques (Macaca assamensis) to see whether males in multimale groups form differentiated social bonds and whether and how males derive fitness benefits from close bonds. We found that strong bonds were linked to coalition formation, which in turn predicted future social dominance, which influenced paternity success. The strength of males' social bonds was directly linked to the number of offspring they sired. Our results show that differentiated social relationships exert an important influence on the breeding success of both sexes that transcends contrasts in relatedness.     

Female sexual swellings in the Asian colobine Simias concolor

During a preliminary study of pig-tailed langurs (Simias concolor) in the Pagai Islands, Indonesia, it was discovered that females exhibited conspicuous swelling of the urogenital triangle. The pig-tailed langur is the first Asiatic colobine found to have prominent sexual swellings and the only colobine with sexual swellings that lives in one-male groups. Because all anthropoids with conspicuous sex skin typically live in groups having female-biased adult sex ratios, it is possible that females might compete amongst themselves for the male in one-male groups, or the best males in multimale groups. Sexual swellings may therefore have resulted from sexual selection for signals attractive to males in female-female competition, as suggested earlier by Bercovitch (California Anthropologist 8:9–12, 1978). Prolonged observation of recognizable individuals will be required to test this hypothesis in the pig-tailed langur and other species.     

The variable social organization of hanuman langurs(Presbytis entellus), infanticide,and the monopolization of females

Data from 24 wild populations of hanuman langurs (Presbytis entellus)in south Asia are used to test hypotheses seeking to explain variation in troop structure and the incidence of infanticide. The occurrence of infanticide is associated with a one-male troop structure and not with a high density. The density, predation, and economic-advantage hypotheses, as explanations for the occurrence of one-male and multimale troops, are not supported by the review. However, the monopolization hypothesis is not contradicted; the number of adult males per troop is significantly correlated with troop size and with the number of adult females per troop. Therefore it is suggested that a one-male troop structure will arise if a male is able to monopolize a group of females, a multimale troop if he cannot. One-male troops may predispose to infanticide because of high variance in male mating success and high intermale competition between groups rather than within troops. If female dispersion determines troop structure, it is speculated that females could manipulate males to form a multimale society if the advantages in terms of infant survival and intertroop conflict exceeded the costs in terms of not producing infanticidal “sexy sons.”     

The effect of male tenure and female mate choice on paternity in free-ranging Japanese macaques

In this study, the paternity of all the infants born in 2002 and 2003 in a free-ranging Japanese macaque (Macaca fuscata) group at Arashiyama in Kyoto, Japan, was analyzed in relation to males' age, dominance rank, and tenure and females' mate choice. The fathers of 20 out of 23 infants were determined by DNA analyses. Central adult (high-ranking) males sired two infants, whereas peripheral adult (low-ranking) males sired 14 infants. Young males sired only one infant. Among adult males, tenure was the most dominant factor that negatively affected male reproductive success. The mating behavior of females who gave birth was also analyzed. The number of male copulations in the peri-fertilization period was positively correlated with the number of infants that they sired. Females copulated with central males with a long tenure only when fertilization was unlikely or impossible. The females probably avoided insemination by males with a long tenure and selected males with a shorter tenure as their mating partners during the ovulation period.     

Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting

Considerable controversy exists concerning possible effects of sexually selected phenotypes via intermale competition on reproductive success. The mandrill ( Mandrillus sphinx ) is an extreme example of evolution by sexual selection, and hence we have studied a semi-free-ranging colony of mandrills in Gabon to gather information on male rank, mating success and paternity, as determined by DNA fingerprinting. Two morphological variants or adult male were identified; 'fatted' males, with maximum secondary sexual coloration, which occupied dominant positions in the social group, and 'non-fatted' males, with muted secondary sexual adornments, smaller testes and lower plasma testosterone levels, which lived as peripheral/solitary individuals. DNA fingerprinting analyses on infants born over five successive years showed that only the two most dominant, fatted males in the group had fathered off spring. Throughout the annual mating season these males attempted to mate-guard and copulate with females during periods of maximal sexual skin tumescence. Male rank and mating success were strongly positively related and the alpha male sired 80–100% of the resulting offspring during three consecutive years. Non-fatted adult males and group associated subadult males engaged in infrequent, opportunistic matings and did not guard females. Loss of alpha status resulted in a fall in reproductive success, but the effect was gradual; the deposed alpha male continued to father 67% and 25% of infants born during the next two years. Thus these results of behavioural and genetic studies on mandrills demonstrate unequivocally that clear-cut relationships exist between male secondary sexual development, social dominance, copulatory behaviour and reproductive success in the social group.     

Male reproductive strategies in black and gold howler monkeys (Alouatta caraya)

Behavioral and demographic factors such as group size, social structure, dispersal patterns, and mating systems affect male reproductive success. In the present study, we analyze the relationship between social structure, genetic relatedness of adult males and offspring paternity in one population of Alouatta caraya inhabiting a continuous forest in Northern Argentina. After 14 months of behavioral studies and genotyping 11 microsatellites, we found that dominant or central males achieved greater mating success and fathered all the offspring conceived during our study in two multimale–multifemale groups (both including three adult males). Although skewed toward the dominant males, females copulated with almost all resident males and with extra group males. We found significantly fewer agonistic interactions between adult males in the group with fewer females and where males were more genetically related to each other (average relatedness r = 0.237; 0.015 int/ind/hr vs. r = 0.02; 0.029 int/ind/hr). Paternity was also analyzed in two other neighboring groups which also showed strong skew to one male over a 2‐year period. These results reveal that even though female black and gold howlers mate with many males, infants are typically fathered by one dominant male. Am. J. Primatol. 76:43–55, 2014. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis

The challenge hypothesis asserts that testosterone levels and aggression in male adult animals are closely associated with one another in the context of intense reproductive competition, particularly when males challenge one another for the access to females. For mantled howler monkeys (Alouatta palliata), the presence of a solitary male in the vicinity of a social group can be considered a threat for the reproductive success of the resident males, as group takeovers by solitary males are followed by a reestablishment of the access to females among group males and sometimes by infanticide. Therefore, these episodes should be accompanied by an increase in testosterone secretion according to the challenge hypothesis. In order to test our prediction, we relate different group and subpopulation variables to the testosterone levels measured in feces collected from 10 groups living in 6 forest fragments, at Los Tuxtlas, Mexico. Our results suggest that resident A. palliata males regard solitary individuals as potential contesters for their reproductive success and that they respond to interactions with them with an increase in testosterone levels, that is increasing their aggressiveness. Our results also suggest that in the studied groups all males have at least certain access to mates and that the entrance of a new male would affect their reproductive success negatively. Finally, the negative effects of chronically high testosterone levels may be negatively affecting the fitness of our study groups living in high population densities and small fragments.