‘O father: where art thou?’— Paternity assessment in an open fission–fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay,Western Australia

Sexually mature male bottlenose dolphins in Shark Bay cooperate by pursuing distinct alliance strategies to monopolize females in reproductive condition. We present the results of a comprehensive study in a wild cetacean population to test whether male alliance membership is a prerequisite for reproductive success. We compared two methods for inferring paternity: both calculate a likelihood ratio, called the paternity index, between two opposing hypotheses, but they differ in the way that significance is applied to the data. The first method, a Bayesian approach commonly used in human paternity testing, appeared to be overly conservative for our data set, but would be less susceptible to assumptions if a larger number of microsatellite loci had been used. Using the second approach, the computer program cervus 2.0, we successfully assigned 11 paternities to nine males, and 17 paternities to 14 out of 139 sexually mature males at 95% and 80% confidence levels, respectively. It appears that being a member of a bottlenose dolphin alliance is not a prerequisite for paternity: two paternities were obtained by juvenile males (one at the 95%, the other at the 80% confidence level), suggesting that young males without alliance partners pursue different mating tactics to adults. Likelihood analyses showed that these two juvenile males were significantly more likely to be the true father of the offspring than to be their half-sibling (P < 0.05). Using paternity data at an 80% confidence level, we could show that reproductive success was significantly skewed within at least some stable first-order alliances (P < 0.01). Interestingly, there is powerful evidence that one mating was incestuous, with one calf apparently fathered by its mother's father (P < 0.01). Our study suggests that the reproductive success of both allied males, and of nonallied juveniles, needs to be incorporated into an adaptive framework that seeks to explain alliance formation in male bottlenose dolphins.     

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.     

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.     

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.     

Long‐term social structure of a resident community of Atlantic spotted dolphins,Stenella Frontalis,in the Bahamas 1991–2002

Long‐term social structure data on small delphinids is lacking for most species except the bottlenose dolphin. This study describes the long‐term social structure of one community of Atlantic spotted dolphins, Stenella frontalis, divided into three social clusters. Data from 12 yr were analyzed using SOCPROG 2.3. Coefficients of association (CoA) were calculated using the half‐weight index. The overall mean community CoA ranged from 0.09 to 0.12. Temporal analyses and mantel tests revealed significant differences between sex class associations due to high male‐male CoA (0.12–0.23) compared to female‐female and mixed sex CoA (0.08–0.10). Female associations were strongly influenced by reproductive status, calf care, and social familiarity, but not by age class. Male associations were strongly influenced by age, access to females, and alliance formation. Males showed two levels of alliance formation, long‐term first order pairs/trios (CoA 0.70–1.00) and shorter‐term second order alliances between two or more first order alliances (CoA 0.45–0.69), and a possible third level during interspecies interactions. Mating strategies, sex, and cluster formation shaped the social structure in this spotted dolphin community. Similar to many bottlenose dolphin studies, long‐term affiliations for spotted dolphins were correlated with age, sex, and reproductive status.     

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.     

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.     

Complex social structure, alliance stability and mating access in a bottlenose dolphin 'super-alliance'

Large brain size in mammals has been related to the number and complexity of social relationships, particularly social alliances within groups. The largest within-group male alliance known outside of humans is found in a social network (> 400) of Indian Ocean bottlenose dolphins (Tursiops aduncus) in Shark Bay Western Australia. Members of this dolphin 'super-alliance' cooperate against other alliances over access to females. Males within the super-alliance form temporary trios and occasionally pairs in order to consort with individual females. The frequent switching of alliance partners suggests that social relationships among males within the super-alliance might be relatively simple and based on an equivalence rule', thereby allowing dolphins to form large alliances without taxing their 'social intelligence'. The equivalence model predicts that the 14 males in the super-alliance should not exhibit differences in alliance stability or partner preferences. However, data from 100 consortships do not support the equivalence hypothesis. The 14 males exhibited striking differences in alliance stability and partner preferences suggesting that the super-alliance has a complex internal structure. Further, within the super-alliance, alliance stability correlates with consortship rate, suggesting that differentiated relationships within the super-alliance are based on competition for access to females.     

Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals

Bottlenose dolphins in Shark Bay, Australia, live in a large, unbounded society with a fission-fusion grouping pattern. Potential cognitive demands include the need to develop social strategies involving the recognition of a large number of individuals and their relationships with others. Patterns of alliance affiliation among males may be more complex than are currently known for any non-human, with individuals participating in 2-3 levels of shifting alliances. Males mediate alliance relationships with gentle contact behaviours such as petting, but synchrony also plays an important role in affiliative interactions. In general, selection for social intelligence in the context of shifting alliances will depend on the extent to which there are strategic options and risk. Extreme brain size evolution may have occurred more than once in the toothed whales, reaching peaks in the dolphin family and the sperm whale. All three 'peaks' of large brain size evolution in mammals (odontocetes, humans and elephants) shared a common selective environment: extreme mutual dependence based on external threats from predators or conspecific groups. In this context, social competition, and consequently selection for greater cognitive abilities and large brain size, was intense.     

Fine-scale sociality reveals female–male affiliations and absence of male alliances in bottlenose dolphins (Tursiops truncatus) in the Shannon Estuary,Ireland

Knowledge of social behavior at an individual level is central to our understanding of complex mammalian societies. In this study, we analyzed the fine-scale sociality of wild bottlenose dolphins in the Shannon Estuary, Ireland, by examining associations between members of the whole population and between specific female and male dolphins. We carried out 51 boat-based individual focal follows on 18 identifiable bottlenose dolphins over 90.8 hr (39 days) between 2014 and 2016. Additionally, we conducted 353 boat-based surveys (with 607 sightings) between 2012 and 2015, and identified 121 distinct adult/juvenile dolphins. The mean group size of focal dolphin groups was 7.2 ± 4.1 (range = 1–20) and the mean fission-fusion rate was 3.06 ± 1.35 changes/hr. The most frequent composition of within-group affiliate pairs was female–male. Focal males spent more time with female nearest-neighbors than male nearest-neighbors (p = .013). Differences between female and male activity budgets were not strongly supported (p = .13). There was no evidence for male alliance formation in the Shannon Estuary population, and all of the known-sex top-ranked associates (7) of known males (n = 10) were females. This research reveals a distinct bottlenose dolphin society with female–male affiliations and an absence of male alliances.     

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.     

Reproductive success in reindeer males in a herd with varying sex ratio

In polygynous species, male reproductive success is often correlated with dominance status of individual males and sex ratio in the population. Reindeer, Rangifer tarandus, is a polygynous species, and here we compared the variation in male reproductive success and dominance status during two successive years in a herd with a male:female sex ratio of 1:7 and 1:3. Copulations were recorded, together with data on male dominance hierarchy and size of mating groups. Male reproductive success was estimated by paternity analysis of calves using microsatellite DNA markers. The distribution of reproductive success among the males was highly skewed for both years with the most dominant male also being the most successful. The largest mating group was established in the herd with the least skew in sex ratio. In this herd some of the adult males present were less reproductively successful than some of the more subordinate younger males. Estimates of the mating group size of males, correcting for dominance status when more than one male is present in the groups, gave good prediction of individual males' reproductive success.     

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.     

Whistle Convergence among Allied Male Bottlenose Dolphins (Delphinidae, Tursiops sp.)

Dolphins are adept at learning new vocalizations (whistles) throughout life, an ability thus far demonstrated in few nonhuman mammals. In dolphins, this ability is well documented in captivity but poorly studied in the wild, and little is known of its role in natural social behavior. This study documents the previously unknown phenomenon of whistle convergence among habituated free-living male bottlenose dolphins ( Tursiops sp.). Over a 4 yr study period, three male subjects formed an alliance, spending most of their time together and cooperating to herd females. Within individuals, whistle repertoires were more variable than expected based on previous studies, mostly performed with captive dolphins, but became less so during the course of the study. Among individuals, the distinctiveness of individual repertoires decreased such that the three males were virtually indistinguishable by the end of the study. Initially, some whistle types were shared. By the end of the study, the three males had formed a close alliance, and had all converged on one particular shared whistle form which they had rarely produced before forming the alliance. The results are discussed in terms of their implications for the prevailing 'signature whistle' hypothesis, as well as possible mechanisms and functional significance of whistle convergence among cooperating males.     

Male reproductive success in plateau pikas (Ochotona curzoniae): A microsatellite analysis

In many social species, competition and cooperation between group members may lead to a large variance in reproductive success among individuals, especially for adult male. From April to August 2002, we studied the adult male reproductive success of plateau pikas in Haibei Alpine Meadow Ecosystem Research Station, Chinese Academy of Science, using microsatellite analysis of paternity, mark-recapture and behavioral observations. Our result indicated that the reproductive success of adult males had a large variance. Its average was 6 individuals and range was from 0 to 13 individuals. One-third of males sired 63.22% offspring. There was a hierarchy system in polygynandrous families. Although the reproductive success of dominant males was higher than that of subordinate males, subordinate males still play an important role in the reproductive success of the population.     

Primate social behavior and ostracism

Ostracism, and its attendant processes, emigration and immigration, are now recognized as basic mechanisms intrinsic to the long-term adaptation of primate society. Ostracism, defined as socially determined exclusion from the resources and opportunities necessary to successful reproduction, is a basic mechanism by which individuals strive to maximize their own reproductive success at the expense of others. Among males this process most often involves exclusion from opportunities to fertilize females (zygote formation) whereas among females it leads to competition for the resources necessary to raise these zygotes to adulthood. Ostracism from intrasexual competition may be so intense that it leads to the migration of less successful individuals into social groups offering greater opportunity. The “passports” most often used in primate immigration are sexual affinity and kinship alliance. Migration carries high risk and is associated with increased mortality and morbidity. Nevertheless, ostracism, emigration, and immigration remain as the basic social processes by which the ratio of resources to individuals shifts and balances from one year to the next. Such adjustments are made through the process of individual “decisions” and “strategies” to optimize personal reproductive success, but their net effect is to constantly redistribute individuals in relation to resources vital to reproduction.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

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.     

Behavioral variation and reproductive success of male baboons (Papio anubis x Papio hamadryas) in a hybrid social group

We take advantage of an array of hybrid baboons (Papio anubis x Papio hamadryas) living in the same social group to explore the causes and consequences of different male mating strategies. Male hamadryas hold one-male units and exhibit a sustained, intense interest in adult females, regardless of the latter's reproductive state. Anubis baboons, by contrast, live in multi-male, multi-female groups where males compete for females only when the latter are estrous. These two taxa interbreed to form a hybrid zone in the Awash National Park, Ethiopia, where previous work has suggested that hybrid males have intermediate and ineffective behavior. Here, we first examine male mating strategies with respect to morphological and genetic measures of ancestry. We found significant relationships between behavioral measures and morphology; males with more hamadryas-like morphology had more hamadryas-like behavior. However, genetic ancestry was not related to behavior, and in both cases intermediates displayed a previously unreported level of behavioral variation. Furthermore, male behavior was unrelated to natal group. Second, we evaluated reproductive success by microsatellite-based paternity testing. The highest reproductive success was found for individuals exhibiting intermediate behaviors. Moreover, over nine years, some genetically and morphologically intermediate males had high reproductive success. We conclude that the behavior of hybrid males is therefore unlikely to be an absolute barrier to admixture in the region.     

Mating system of the Eurasian badger, Meles meles, in a high density population

Badgers are facultatively social, forming large groups at high density. Group-living appears to have high reproductive costs for females, and may lead to increased levels of inbreeding. The extent of female competition for reproduction has been estimated from field data, but knowledge of male reproductive success and the extent of extra-group paternity remains limited. Combining field data with genetic data (16 microsatellite loci), we studied the mating system of 10 badger social groups across 14 years in a high-density population. From 923 badgers, including 425 cubs, we were able to assign maternity to 307 cubs, with both parents assigned to 199 cubs (47%) with 80% confidence, and 14% with 95% confidence. Age had a significant effect on the probability of reproduction, seemingly as a result of a deficit of individuals aged two years and greater than eight years attaining parentage. We estimate that approximately 30% of the female population successfully reproduced in any given year, with a similar proportion of the male population gaining paternity across the same area. While it was known there was a cost to female reproduction in high density populations, it appears that males suffer similar, but not greater, costs. Roughly half of assigned paternity was attributed to extra-group males, the majority of which were from neighbouring social groups. Few successful matings occurred between individuals born in the same social group (22%). The high rate of extra-group mating, previously unquantified, may help reduce inbreeding, potentially making philopatry a less costly strategy.