Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies

Male bottlenose dolphins (Tursiops sp.) in Shark Bay have one of the most complex male societies outside humans. Two broad mating strategies have been identified in males. In the first strategy, there are two types of alliances: stable 'first-order' pairs and trios that herd individual females in reproductive condition, and 'second-order' teams of two first-order alliances (five or six individuals) that join forces against rivals in contests for females. In the alternative strategy, a 'super-alliance' of ca. 14 individuals, males form pairs or trios to herd females, but in contrast to the stable alliances, these pairs and trios are highly labile. Here, we show that males in stable first-order alliances and the derived second-order alliances are often strongly related, so that they may gain inclusive fitness benefits from alliance membership. By contrast, members of the super-alliance are no more closely related than expected by chance. Further, the strength of the association of alliance partners within the super-alliance, as measured by an index of joint participation in consorting a female, was not correlated with their genetic relatedness. Thus, within one population and one sex, it appears that there may be simultaneous operation of more than one mode of group formation.     

Dominance, aggression and reproduction in primate societies

Dominance relationships in primate societies are generally inferred by analyses of agonistic interactions. This aspect of social organization is so striking in macaque and baboon societies that many theoreticians have postulated selective mechanisms operating on the genetic attributes which contribute to high dominance rank. Alpha males were hypothesized to increase their genetic fitness by successfully competing with other males for access to ovulating females.Evidence relevant to these speculations has been mixed. Whereas some investigators found alpha males had near exclusive sexual access to females, others failed to confirm preferential access to ovulating females. Indeed, considerable variability in competition for females existed not only among species, but also among troops of the same species living in different habitats. Further, partner selection was not an exclusive male prerogative; females proved to express active preferences for particular males as sexual partners, and these preferences were not related to high male aggressivity.Alpha males, however, were noted to maintain their positions through social skills as members of a central core or alliance, and high rank was related primarily to seniority. Moreover, alpha males responded actively to challenges to the troop and were judged to contribute significantly to the survival of infants. It was therefore hypothesized that increased genetic fitness related to the increased survival of immature animals in the troop, most of which would already be the offspring of senior (and hence alpha) males. Selection would then be for the social skills leading to successful alliances in troop defense. Such skills might also relate to female partner preferences thus increasing the reproductive effectiveness of alpha males at any point in their careers, including years prior to and following their assumption of alpha rank.     

A new level of complexity in the male alliance networks of Indian Ocean bottlenose dolphins (Tursiops sp.)

Male bottlenose dolphins in Shark Bay, Western Australia form two levels of alliances; two to three males cooperate to herd individual females and teams of greater than three males compete with other groups for females. Previous observation suggested two alliance tactics: small four to six member teams of relatives that formed stable pairs or trios and unrelated males in a large 14-member second-order alliance that had labile trio formation. Here, we present evidence for a third level of alliance formation, a continuum of second-order alliance sizes and no relationship between first-order alliance stability and second-order alliance size. These findings challenge the 'two alliance tactics' hypothesis and add to the evidence that Shark Bay male bottlenose dolphins engage in alliance formation that likely places considerable demands on their social cognition.     

Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Bottlenose dolphins are one of only a few mammalian taxa where the males are known to cooperate within their social group in order to maintain mating access to single females against other males. Male bonds in bottlenose dolphins have been hypothesized as evolving through kinship and associated inclusive fitness effects. In this study we tested whether individually identified male bottlenose dolphins preferentially associate and form alliances with kin in a small coastal resident population of southeastern Australia using a combination of behavioural data, genetic sexing, sequences of the mitochondrial DNA control region and nuclear microsatellite markers. Males generally associated significantly more often than expected with one to three other males, with whom they jointly herded females for mating. Associations and alliance membership were not associated with either maternal kinship or genetic relatedness. The majority of male pairs within alliances were randomly related, although high relatedness values were found between males of different alliances in the resident population. These findings indicate that mechanisms other than kin selection may be foremost in the development and maintenance of cooperation between male bottlenose dolphins.     

Synchrony,leadership, and association in male Indo-pacific bottlenose dolphins (Tursiops aduncus)

Male Indo-pacific bottlenose dolphins in Shark Bay, Western Australia, have converged with humans in the formation of nested male alliances and the use of synchrony in alliance behavior. Further, the strength of association among allied male dolphins varies and the stability of alliances correlates with the rate that males consort with estrus females (and is thus a possible indicator of dominance). To examine the possibility that synchrony reflects alliance association strength and dominance relationships, we analyzed videotapes from focal follows of two groups of males that reflect the range of alliance size and the strength of association between individuals in the population. We examined two variables: leadership during synchronous behaviors, based on which animal in a synchronously surfacing pair surfaced first, and the degree of synchrony, based on temporal differences in synchronous surfacing. We predicted that closer associates would exhibit a greater degree of synchrony and that one dolphin in a dyad would consistently lead. Contrary to our predictions, the degree of synchrony was inversely related to strength of association within alliances. This surprising result suggests that individuals with less secure bonds may strive more to achieve synchrony. We found no evidence of leadership during synchronous surfacing or between synchrony and other behavioral variables. Proximate mechanisms for synchronous behavior, such as entrainment and mutual motor imitation (“the mirror game” paradigm), may inhibit leadership in this context. Our results show that synchrony during surfacing is not a useful behavior to examine for dominance relationships in wild dolphins but it may be a useful tool to examine variation in alliance relationships.     

A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): complex male alliances in an open social network

Terrestrial mammals with differentiated social relationships live in 'semi-closed groups' that occasionally accept new members emigrating from other groups. Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia, exhibit a fission-fusion grouping pattern with strongly differentiated relationships, including nested male alliances. Previous studies failed to detect a group membership 'boundary', suggesting that the dolphins live in an open social network. However, two alternative hypotheses have not been excluded. The community defence model posits that the dolphins live in a large semi-closed 'chimpanzee-like' community defended by males and predicts that a dominant alliance(s) will range over the entire community range. The mating season defence model predicts that alliances will defend mating-season territories or sets of females. Here, both models are tested and rejected: no alliances ranged over the entire community range and alliances showed extensive overlap in mating season ranges and consorted females. The Shark Bay dolphins, therefore, present a combination of traits that is unique among mammals: complex male alliances in an open social network. The open social network of dolphins is linked to their relatively low costs of locomotion. This reveals a surprising and previously unrecognized convergence between adaptations reducing travel costs and complex intergroup-alliance relationships in dolphins, elephants and humans.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Universal sex differences in online advertisers age preferences: comparing data from 14 cultures and 2 religious groups

The search for a potential partner has been aided over recent years by the widespread use of online dating sites and this process of relationship formation has conveniently presented an ideal opportunity for researchers to analyze human mating desires and to compare evolutionary and social constructivist based hypotheses. One such aspect of human mating behaviour yet to be thoroughly explored using access to online dating advertisements is the idealized age desired by each sex when considering a possible relationship. This study accessed minimum (youngest age considered) and maximum (oldest age considered) age preferences from 14 separate cultures and two religious groups from both sexes at ages 20, 25, 30, 35, 40, 45, and 50 years. The results showed that overall there was a growing disparity between males own age and preferred age of partner as males themselves aged (as indicated by greater effect sizes with advertisers age), with females showing a pattern for preferences around their own age or older. Females did not express an age preference for males younger than male's age preferences for females at any advertiser's age. On only three occasions were there no age differences between the sexes in their desire to initiate a relationship with the opposite sex. The results were clearly concurrent with earlier findings supportive of evolutionary or adaptationist interpretations. Neither a random pattern of age preferences more consistent with an arbitrary norms prediction, nor clear evidence for toy boy proclivities in females or males was found. Future studies utilizing the methodology used in this study to examine other human mating decision making processes are proposed.     

Male reproductive success increases with alliance size in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

1. Determining the extent of variation in male mating strategies and reproductive success is necessary to understand the fitness benefits of social and cooperative behaviour. 2. This study assesses the reproductive success of male Indo-Pacific bottlenose dolphins in a small embayment population where different behavioural strategies of males have previously been identified. Parentage for 44 sampled calves was examined using 23 microsatellite loci and one mitochondrial DNA marker. Our candidate parent pool of 70 males and 64 females contained individuals sampled from both the embayment and adjacent coastal populations. 3. A moderate level of polygyny was detected in our sample. We assigned paternity of 23 calves to 12 males at the strict 95% confidence level and an additional nine calves to two males at the 80% confidence level. The majority (92%) of successful males were identified as residents to the embayment, and 46% of offspring were located within the same social group or community as their father. 4. Our results suggest that the size of alliances was the best predictor of reproductive success for males in this population, while the strength of association among allied males, alliance stability and male ranging patterns had little influence. In line with predictions for male alliances formed between unrelated individuals, we found that reproductive skew within alliances was not large. 5. Together, our genetic and behavioural analyses demonstrate that alliance formation between male dolphins is a successful strategy to enhance reproductive output.     

Familiarity and partner preferences in female common voles, <Emphasis Type="Italic">Microtus arvalis</Emphasis>

Captive female common voles (Microtus arvalis) had a clear social preference for familiar males in a standard preference test. Cohabitation for a short period resulted in preferences for familiar partners, and females spent eight times more time in body contact with a familiar male than with an unfamiliar male. Females also displayed stranger-directed aggression. Our results suggest that the common vole is a species with selective partner preferences and a tendency to form tight social relationships and stable male–female associations.     

Stability and Durability of Intra- and Intersex Social Bonds of Captive Rhesus Macaques (Macaca mulatta)

Many social species maintain differentiated relationships with their group members. These social bonds may reflect short-term interactions satisfying immediate needs. Alternatively, individuals of some species may entertain stable and valuable bonds that last much longer than opportunistic interactions would predict. This claim is supported by recent research that revealed clear fitness benefits for long-lasting social bonds. Here, we investigated the stability and equitability of social relationships in captive rhesus macaques, measured using their proximity and grooming patterns over a 3-yr period. We show that, in general, proximity patterns of the whole group were stable over 3 yr. More specifically, each individual’s top two nonkin within and between sex relationships based on proximity were relatively stable and some of these relationships lasted the full 3 yr. Female grooming relationships within and between sex were also stable over 3 yr. Moreover, strong social bonds in females were not based on age similarity and were not sex specific, suggesting that a general underlying mechanism of social bonding in female rhesus macaques. In contrast, patterns of male grooming of other males and of females were relatively unstable and male social bonds were less equitable than those of females. The differences in stability of the relationships between the sexes may reflect the dispersal pattern of rhesus macaques, although we have limited data on non-natal males in our study. With these data we add to a growing body of literature describing the value and durability of relationships among primates and other species.     

Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata)

Studies of social affiliation and social spacing offer important insight into the dynamics of subgroup formation and social strategies in living primates. Among the 11 species in the genus Alouatta, mantled howlers (A. palliata) are the only species to consistently form large, stable social groups composed of several adult males and several adult females. In this study, we examine patterns of subgrouping, activity, and partner preferences in a troop of 26-29 wild mantled howling monkeys (including 12-13 marked individuals) inhabiting Isla de Ometepe, Nicaragua. During two study seasons in 2000 and 2001, we simultaneously monitored the size, composition, and activities of individuals in two to three different subgroups. A half-weight association index was used to calculate partner preferences and patterns of spatial association. Results indicate that our howler study troop fragmented into subgroups of 1-20 with subgroups averaging five and six individuals. Subgroup size and membership reflected individual patterns of social affiliation and social tolerance, and in general remained consistent across activities and from year to year. We also found evidence of cliques or social networks of three to four individuals embedded within larger subgroups. A small number of adult males appeared to play an important social role as the nucleus of clique formation. We argue that the persistence of strong male-male and male-female partner preferences in mantled howlers helps to explain the stability of relatively large multimale-multifemale groups.     

Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra)

We investigated the social and hormonal mechanisms underlying male reproductive strategies in two multimale-multifemale groups of black howler monkeys (Alouatta pigra) during a 14-month study in Palenque National Park, Mexico. Fecal glucocorticoid (fGC) and androgen (fA) levels were analyzed for 343 fecal samples collected from 14 males during their presence in the study groups. Neither immigrating males nor resident males that remained in the group had elevated fGC and fA levels during 11 observed male migration events, suggesting that competition over group membership was not associated with variation in the fecal hormonal levels of males. Instead, fGC and fA levels were significantly higher in males who maintained a central position in the group and had almost exclusive access to fertile females than in other resident males. These “central” males were responsible for maintaining close spatial associations and cultivating strong affiliative relationships with cycling, sexually active females but not with noncycling, sexually inactive females. “Noncentral” males did not form strong social relationships with either cycling or noncycling females and had no or very few mating opportunities. Our findings suggest that male black howler monkeys compete nonaggressively by fostering relationships with cycling females and that the elevated fGC levels of central males may be indicative of the social challenges involved in their indirect competition.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. II. Influence of Male Rank and Possible Competition for Partners

Allogrooming contributes to the development and maintenance of social relationships, including those that involve alliances, in many primate species. Variation in relatedness, dominance rank, and other factors can produce variation in the value of others as grooming partners. Several models have been developed to account for variation in the distribution of grooming in relation to dominance ranks. These start from the premise that individuals are attracted to high-ranking partners, but time limits, direct competition, and prior grooming engagement between high-ranking individuals can constrain access to them. Sambrook et al. (1995) formalized some of these models and showed the importance of taking group size variation into account when assessing them. Chimpanzees form multimale communities in which males are the philopatric sex. Males commonly associate and groom with each other; they also form dominance hierarchies and form alliances that influence dominance ranks and mating success. Both male rank and the rank distance between partners are significantly correlated with the distribution of grooming between males in an extremely large chimpanzee community at Ngogo, Kibale National Park, Uganda, that has more males than any other known community. High-ranking males had more grooming partners than mid- or low-ranking males. Grooming predominantly went up the dominance hierarchy, but was also concentrated among males that were close in rank. Rank and rank distance apparently both affected grooming independently of reciprocity in grooming and independently of the frequency with which males associated in temporary parties. However, the data do not clearly indicate how constraints on access to partners might have operated. Published data from a smaller chimpanzee community at Mahale show no rank or rank distance effect on male grooming. These results and earlier, conflicting findings on the association between dominance rank and grooming in male chimpanzees indicate that variation in group size, i.e., the number of males per community, probably influences the strength of any such effects, as happens for grooming between females in several cercopithecine species. Data on coalitions at Ngogo support the argument that high-ranking males are valuable social partners, and similarity in strategies of alliance formation may influence the distribution of grooming.     

Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra

Patterns of agonistic and nonagonistic behaviors were studied in a troop of wild pig-tailed macaques in West Sumatra, Indonesia. The animals were provisioned and the identities of all adult and adolescent individuals were known. The females could be divided into high-, mid-, and low-ranking subsets of individuals. Most grooming occurred within, instead of between members of these subsets. The members of each subset also tended to feed together at the baiting sites, and they probably represented groups of close kin. Among females, grooming appeared to be a conciliatory behavior and was generally performed by the subordinate partner, while mounting was performed by the dominant partner and appeared to be a reassertion of dominance. High-ranking males tended to form agonistic alliances with females and to exchange grooming with estrous females. Low-ranking males did not have such associations with females and were frequently the targets of agonistic alliances of females and juveniles. Mounting between males appeared to be a conciliatory behavior. It seemed effective since severe aggression between males was not observed. The subordinate partner mounted more frequently than the dominant one, but the direction of mounting was apparently controlled by the latter. This suggests that, among pig-tailed macaques, the dominant male plays an important role in the coexistence of males in the troop.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Social structure of Atlantic spotted dolphins,Stenella frontalis,following environmental disturbance and demographic changes

Extreme environmental events and demographic changes can have variable effects on the social structure of animal populations. This study compared the social structure of a community of Atlantic spotted dolphins in the Bahamas before and after two hurricanes. Approximately 36% of the individuals were lost, with no subsequent increase in immigration. The majority of the social structure characteristics were consistent with results from a long‐term study covering the previous 12 yr, including community structure with definitive social clusters, sex preferences and overall association patterns. However some changes occurred, though still constrained within sex preferences. Posthurricane there was a decrease in social differentiation and increased cohesion within clusters and across age class. Males retained or made new first order alliances, however, only one second order alliance was evident, revealing a simplified alliance structure. Juvenile individuals made alliance level associations, unprecedented from long‐term analysis. Although other studies have shown stark restructuring, this study showed that less drastic changes within overall social structure stability can occur. Persistence and evolutionary changes in populations through environmental and/or demographic perturbations may depend on the social structure of a population or community. Understanding the processes involved in social development is paramount for conservation of diverse populations.     

Development of partner preferences in Japanese Macaques (Macaca fuscata): Effects of gender and kinship during the second year of life

Quantitative data are presented on the effects of subject sex, partner sex,and kinship on the social interactions of 18 juveniles of the Oregon troop of Japanese macaques (Macaca fuscata).Data on these subjects as infants were also used to detail maturational changes in partner sex preferences. Nine males and nine females, whose multiparous mothers represented a cross section of dominance ranks, were observed using a focal-animal technique. Juveniles of both sexes engaged in more proximity, contact, grooming, mounting, aggression, and social play with kin than with nonkin partners. They initiated less contact with females and more contact with males during their second year. They initiated more grooming and aggression during their second year than their first year, with females displaying a strong preference for grooming females and males specifically aggressing males more during the second year. Aggression was higher between same-sexed partners than between opposite-sexed partners. Males engaged in more social interactions with males during the second year than the first year of life. Males played more than females during both years. Males played more with males during the second year than the first year, and males played with males more than did females during the second year. We conclude that sex differences in behavioral frequencies become evident during the first year of life, and sex differences in partner preferences emerge during the second year of life.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.     

Effects of natal male alliances on aggression and power dynamics in rhesus macaques

In the wild, male rhesus macaques disperse at sexual maturity. In captivity, however, males cannot disperse from their natal groups. Thus, the presence of natal males in captive rhesus social groups is unnatural and has the potential to negatively influence group dynamics and stability. A primary difference between natal males and non-natal (immigrant) males is that natal males have the opportunity to form long-term alliances with their maternal kin as well as nonkin. We investigated the factors associated with natal males' kin alliances and the impact of these alliances on measures of natal male behavior, group dynamics, and group stability. We found that natal males more frequently formed alliances with maternal kin when they were from high-ranking matrilines, had more siblings, and were younger. More frequent kin alliances were associated with more frequent use of intense aggression, higher individual rank, and higher degree of integration within the male displacement network. Thus, it seems that natal males use their alliances to be more active and influential in the social group, which may affect group stability. It appears that juvenile natal males from high-ranking matrilines, in particular, have the largest impact on group stability. Younger natal males from high-ranking matrilines formed alliances with kin more frequently and used intense aggression more frequently than older or lower ranking males. Furthermore, groups with a higher proportion of juvenile males from high-ranking matrilines also had higher rates of wounding. We suggest that the presence of natal males in rhesus groups may act in opposition to group stability.