Juvenile social play predicts adult reproductive success in male bottlenose dolphins.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.

Strategic intergroup alliances increase access to a contested resource in male bottlenose dolphins.

Efforts to understand human social evolution rely largely on comparisons with nonhuman primates. However, a population of bottlenose dolphins in Shark Bay, Western Australia, combines a chimpanzee-like fission-fusion grouping pattern, mating system, and life history with the only nonhuman example of strategic multilevel male alliances. Unrelated male dolphins form three alliance levels, or "orders", in competition over females: both within-group alliances (i.e., first- and second-order) and between-group alliances (third-order), based on cooperation between two or more second-order alliances against other groups. Both sexes navigate an open society with a continuous mosaic of overlapping home ranges. Here, we use comprehensive association and consortship data to examine fine-scale alliance relationships among 121 adult males. This analysis reveals the largest nonhuman alliance network known, with highly differentiated relationships among individuals. Each male is connected, directly or indirectly, to every other male, including direct connections with adult males outside of their three-level alliance network. We further show that the duration with which males consort females is dependent upon being well connected with third-order allies, independently of the effect of their second-order alliance connections, i.e., alliances between groups increase access to a contested resource, thereby increasing reproductive success. Models of human social evolution traditionally link intergroup alliances to other divergent human traits, such as pair bonds, but our study reveals that intergroup male alliances can arise directly from a chimpanzee-like, promiscuous mating system without one-male units, pair bonds, or male parental care.

Inter-group alliance dynamics in Indo-Pacific bottlenose dolphins (Tursiops aduncus).

The social intelligence hypothesis holds that complex social relationships are the major selective force underlying the evolution of large brain size and intelligence. Complex social relationships are exemplified by coalitions and alliances that are mediated by affiliative behavior, resulting in differentiated but shifting relationships. Male Indo-Pacific bottlenose dolphins in Shark Bay, Australia, form three alliance levels or 'orders', primarily among non-relatives. Strategic alliance formation has been documented within both first- and second-order alliances and between second-order alliances ('third-order alliances'), revealing that the formation of strategic inter-group alliances is not limited to humans. Here we conducted a fine-scale study on 22 adult males over a 6-year period to determine if third-order alliance relationships are differentiated, and mediated by affiliative interactions. We found third-order alliance relationships were strongly differentiated, with key individuals playing a disproportionate role in maintaining alliances. Nonetheless, affiliative interactions occurred broadly between third-order allies, indicating males maintain bonds with third-order allies of varying strength. We also documented a shift in relationships and formation of a new third-order alliance. These findings further our understanding of dolphin alliance dynamics and provide evidence that strategic alliance formation is found in all three alliance levels, a phenomenon with no peer among non-human animals.

Association patterns and community structure among female bottlenose dolphins: environmental, genetic and cultural factors.

Social structuring from assortative associations may affect individual fitness, as well as population-level processes. Gaining a broader understanding of social structure can improve our knowledge of social evolution and inform wildlife conservation. We investigated association patterns and community structure of female Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, assessing the role of kinship, shared culturally transmitted foraging techniques, and habitat similarity based on water depth. Our results indicated that associations are influenced by a combination of uni- and biparental relatedness, cultural behaviour and habitat similarity, as these were positively correlated with a measure of dyadic association. These findings were matched in a community level analysis. Members of the same communities overwhelmingly shared the same habitat and foraging techniques, demonstrating a strong homophilic tendency. Both uni- and biparental relatedness between dyads were higher within than between communities. Our results illustrate that intraspecific variation in sociality in bottlenose dolphins is influenced by a complex combination of genetic, cultural, and environmental aspects. Supplementary Information: The online version contains supplementary material available at 10.1007/s42991-022-00259-x.

Separating overlapping echolocation: An updated method for estimating the number of echolocating animals in high background noise levels.

Much can be learned by investigating the click trains of odontocetes, including estimating the number of vocalizing animals and comparing the acoustic behavior of different individuals. Analyzing such information gathered from groups of echolocating animals in a natural environment is complicated by two main factors: overlapping echolocation produced by multiple animals at the same time, and varying levels of background noise. Starkhammar et al. [(2011a). Biol. Lett. 7(6), 836-839] described an algorithm that measures and compares the frequency spectra of individual clicks to identify groups of clicks produced by different individuals. This study presents an update to this click group separation algorithm that improves performance by comparing multiple click characteristics. There is a focus on reducing error when high background noise levels cause false click detection and recordings are of a limited frequency bandwidth, making the method applicable to a wide range of existing datasets. This method was successfully tested on recordings of free-swimming foraging dolphins with both low and high natural background noise levels. The algorithm can be adjusted via user-set parameters for application to recordings with varying sampling parameters and to species of varying click characteristics, allowing for estimates of the number of echolocating animals in free-swimming groups.

Acoustic coordination by allied male dolphins in a cooperative context.

Synchronous displays are hallmarks of many animal societies, ranging from the pulsing flashes of fireflies, to military marching in humans. Such displays are known to facilitate mate attraction or signal relationship quality. Across many taxa, synchronous male displays appear to be driven by competition, while synchronous displays in humans are thought to be unique in that they serve a cooperative function. Indeed, it is well established that human synchrony promotes cooperative endeavours and increases success in joint action tasks. We examine another system in which synchrony is tightly linked to cooperative behaviour. Male bottlenose dolphins form long-lasting, multi-level, cooperative alliances in which they engage in coordinated efforts to coerce single oestrus females. Previous work has revealed the importance of motor synchrony in dolphin alliance behaviour. Here, we demonstrate that allied dolphins also engage in acoustic coordination whereby males will actively match the tempo and, in some cases, synchronize the production of their threat vocalization when coercing females. This finding demonstrates that male dolphins are capable of acoustic coordination in a cooperative context and, moreover, suggests that both motor and acoustic coordination are features of coalitionary behaviour that are not limited to humans.

Vocal behaviour of allied male dolphins during cooperative mate guarding.

Coercive mate guarding, where males use aggression to control female movements, is a form of sexual coercion which functions to constrain female mate choice. Non-human primates, for example, herd females to keep them away from competing males, but male bottlenose dolphins (Tursiops aduncus) also herd females to keep them close to their alliance partners. Indeed, pairs and trios of male dolphins work together to sequester single estrus females and defend them from competing alliances. Yet how males facilitate such coordination remains unknown. Here, we investigate the vocal behaviour of allied male bottlenose dolphins during the herding of individual females, examining how the production of whistles and 'pops' (a threat vocalisation) varied with behavioural state and inter-animal distances. Allied males produced both whistles and pops significantly more often and at higher rates during social interactions, though they differed in function. Whistle rates increased significantly when new individuals joined the consorting group, consistent with previous work showing that whistles are part of a greeting sequence for this species. Whistle matching also appeared to play a role in within-alliance coordination. Pop vocalisations increased significantly when the nearest male to the female changed, likely inducing the female to remain close as the males coordinate a guard switch. Building upon prior research examining female movements in response to pops, we show that males approach the female and current guard whilst popping, leading to a guard switch. Our results provide new insights into the use of vocal signals during cooperative mate guarding between allied male dolphins.

Cooperation or dolphin 'tug-of-war'? Comment on Kuczaj et al. and Eskelinen et al.

Two recent papers by Kuczaj et al. (Anim Cognit 18:543-550, 2015) and Eskelinen et al. (Anim Cognit 19:789-797, 2016) claim to have demonstrated that (i) bottlenose dolphins (Tursiops truncatus) cooperated to solve a novel task and (ii) vocal signals were important for coordinating these cooperative efforts. Although it is likely that bottlenose dolphins may share communicative signals in order to achieve a common goal, we suggest that this has not been demonstrated in the aforementioned studies. Here, we discuss the two main problems that preclude any definitive conclusions being drawn on cooperative task success and vocal communication from these studies. The first lies in the experimental design. The 'cooperative task', involving an apparatus that requires two dolphins to pull in opposite directions in order to achieve a food reward, is not conducive to cooperation, but could instead reflect a competitive 'tug-of-war'. It is therefore of questionable use in distinguishing competitive from cooperative interactions. Second, the suggestion that the occurrence of burst-pulsed signals in this task was indicative of cooperation is disputable, as (i) this study could not determine which dolphins were actually producing the signals and (ii) this sound type is more commonly associated with aggressive signalling in dolphins. We commend the authors for investigating this exciting and topical area in animal communication and cognition, but the question of whether dolphins cooperate and communicate to solve a cooperative task remains as yet unanswered.

In pop pursuit: social bond strength predicts vocal synchrony during cooperative mate guarding in bottlenose dolphins.

Vocal communication is an emblematic feature of group-living animals, used to share information and strengthen social bonds. Vocalizations are also used to coordinate group-level behaviours in many taxa, but little is known of the factors that may influence vocal behaviour during cooperative acts. Allied male Indo-Pacific bottlenose dolphins (Tursiops aduncus) use the 'pop' vocalization as a coercive signal when working together to herd single oestrous females. Using long-term association and acoustic data, we examined the influence of social and non-social factors on pop use by allied male dolphins in this context. Neither pop rate nor pop bout duration were influenced by any of the factors examined. However, allied males with stronger social bonds engaged in higher rates of vocal synchrony; whereby they actively matched the timing of their pop production. Hence, social bond strength influenced pop use in a cooperative context, suggesting dual functions of pop use: to induce the female to remain close, and to promote social bond maintenance and cooperation among males. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Communication range predicts dolphin alliance size in a cooperative mating system.

It is well known that communication range, often termed active space,1 varies with habitat structure, and this variation can influence individual vocal behavior across taxa.2,3 While theoretical predictions imply that communication distances can drive the evolution of mammalian alliance sizes,4 empirical tests of this hypothesis are currently lacking. In Shark Bay, Western Australia, unrelated male bottlenose dolphins form multilevel alliances, where males work together in pairs or trios to herd single estrus females.5,6,7,8 Here, we use empirical measures of male dolphin vocalizations, ambient noise levels, and high-resolution bathymetry data to estimate variation in active space across the study site. We combine this with long-term data on male alliance behavior to determine how active space influences alliance group size and mating success. We show that the active space of vocalizations used by allied males in a reproductive context predicts the number of preferred alliance partners with whom individuals cooperate over the longer term, ultimately contributing significantly to male access to mating opportunities. These results reveal that variation in sensory ecology driven by heterogeneous habitat influences optimal cooperative group size and mating success within a single population of wild animals.

Social and genetic interactions drive fitness variation in a free-living dolphin population.

The evolutionary forces that drive fitness variation in species are of considerable interest. Despite this, the relative importance and interactions of genetic and social factors involved in the evolution of fitness traits in wild mammalian populations are largely unknown. To date, a few studies have demonstrated that fitness might be influenced by either social factors or genes in natural populations, but none have explored how the combined effect of social and genetic parameters might interact to influence fitness. Drawing from a long-term study of wild bottlenose dolphins in the eastern gulf of Shark Bay, Western Australia, we present a unique approach to understanding these interactions. Our study shows that female calving success depends on both genetic inheritance and social bonds. Moreover, we demonstrate that interactions between social and genetic factors also influence female fitness. Therefore, our study represents a major methodological advance, and provides critical insights into the interplay of genetic and social parameters of fitness.

An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus).

Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These 'epigenetic clocks' present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.

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.

Social and vocal complexity in bottlenose dolphins.

Bottlenose dolphins are highly social, renowned for their vocal flexibility, and possess highly enlarged brains relative to their body size. Here, we discuss some of the defining features of bottlenose dolphin social and vocal complexity and place this in the context of their cognitive evolution.

Bottlenose dolphin communication during a role-specialized group foraging task.

A division of labor with role specialization is defined as individuals specializing in a subtask during repetitions of a group task. While this behavior is ubiquitous among humans, there are only four candidates found among non-eusocial mammals: lions, mice, chimpanzees, and bottlenose dolphins. Bottlenose dolphins in the Cedar Keys, Florida, engage in role specialized "driver-barrier feeding", where a "driver" dolphin herds mullet towards "barrier" dolphins. Thus trapped, the mullet leap out of the water where the dolphins catch them in air. To investigate whether dolphins use acoustic cues or signals to coordinate this behavior, vocalizations were recorded before and during driver-barrier feeding. Results of fine-scale audio and video analysis during 81 events by 7 different driver individuals suggest that barrier animals coordinate movements during these events by cueing on the driver's echolocation. Analysis of dolphin whistle occurrence before driving events versus another foraging technique, which does not involve role specialization, revealed significantly higher whistle production immediately prior to driver-barrier events. Possible whistle functions include signaling motivation, recruiting individuals to participate, and/or behavioral coordination. While the use of cues and signals is common in humans completing role-specialized tasks, this is the first study to investigate the use of vocalizations in the coordination of a role-specialized behavior in a non-human mammal.

Social integration influences fitness in allied male dolphins.

Understanding determinants of differential reproductive success is at the core of evolutionary biology because of its connection to fitness. Early work has linked variation in reproductive success to differences in age,1 rank,2 or size,3,4 as well as habitat characteristics.5 More recently, studies in group-living taxa have revealed that social relationships also have measurable effects on fitness.6-8 The influence of social bonds on fitness is particularly interesting in males who compete over reproductive opportunities. In Shark Bay, Western Australia, groups of 4-14 unrelated male bottlenose dolphins cooperate in second-order alliances to compete with rival alliances over access to females.9-12 Nested within second-order alliances, pairs or trios of males, which can vary in composition, form first-order alliances to herd estrus females. Using 30 years of behavioral data, we examined how individual social factors, such as first-order alliance stability, social connectivity, and variation in social bond strength within second-order alliances, affect male fitness. Analyzing the reproductive careers of 85 males belonging to 10 second-order alliances, we found that the number of paternities a male achieved was positively correlated with his cumulative social bond strength but negatively correlated with his variation in bond strength. Thus, well-integrated males with more homogeneous social bonds to second-order allies obtained most paternities. Our findings provide novel insights into the fitness benefits of polyadic cooperation among unrelated males and highlight the adaptive value of social bonds in this context.

Allied male dolphins use vocal exchanges to "bond at a distance".

Vocal interactions are intrinsic features of social groups and can play a pivotal role in social bonding.1,2 Dunbar's social bonding hypothesis posits that vocal exchanges evolved to "groom at a distance" when social groups became too large or complex for individuals to devote time to physical bonding activities.1,3 Tests of this hypothesis in non-human primates, however, suggest that vocal exchanges occur between more strongly bonded individuals that engage in higher grooming rates4-7 and thus do not provide evidence for replacement of physical bonding. Here, we combine data on social bond strength, whistle exchange frequency, and affiliative contact behavior rates to test this hypothesis in wild male Indo-Pacific bottlenose dolphins, who form multi-level alliances that cooperate over access to females.8-10 We show that, although whistle exchanges are more likely to occur within the core alliance, they occur more frequently between those males that share weaker social bonds, i.e., between core allies that spend less time together, while the opposite occurs for affiliative physical contact behavior. This suggests that vocal exchanges function as a low-cost mechanism for male dolphins that spend less time in close proximity and engage in fewer affiliative contact behaviors to reinforce and maintain their valuable alliance relationships. Our findings provide new evidence outside of the primate lineage that vocal exchanges serve a bonding function and reveal that, as the social bonding hypothesis originally suggested, vocal exchanges can function as a replacement of physical bonding activities for individuals to maintain their important social relationships.

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.

Cooperation-based concept formation in male bottlenose dolphins.

In Shark Bay, Western Australia, male bottlenose dolphins form a complex nested alliance hierarchy. At the first level, pairs or trios of unrelated males cooperate to herd individual females. Multiple first-order alliances cooperate in teams (second-order alliances) in the pursuit and defence of females, and multiple teams also work together (third-order alliances). Yet it remains unknown how dolphins classify these nested alliance relationships. We use 30 years of behavioural data combined with 40 contemporary sound playback experiments to 14 allied males, recording responses with drone-mounted video and a hydrophone array. We show that males form a first-person social concept of cooperative team membership at the second-order alliance level, independently of first-order alliance history and current relationship strength across all three alliance levels. Such associative concepts develop through experience and likely played an important role in the cooperative behaviour of early humans. These results provide evidence that cooperation-based concepts are not unique to humans, occurring in other animal societies with extensive cooperation between non-kin.

Cooperative partner choice in multi-level male dolphin alliances.

Investigations into cooperative partner choice should consider both potential and realised partners, allowing for the comparison of traits across all those available. Male bottlenose dolphins form persisting multi-level alliances. Second-order alliances of 4-14 males are the core social unit, within which 2-3 males form first-order alliances to sequester females during consortships. We compared social bond strength, relatedness and age similarity of potential and realised partners of individual males in two age periods: (i) adolescence, when second-order alliances are formed from all available associates, and (ii) adulthood, when first-order allies are selected from within second-order alliances. Social bond strength during adolescence predicted second-order alliance membership in adulthood. Moreover, males preferred same-aged or older males as second-order allies. Within second-order alliances, non-mating season social bond strength predicted first-order partner preferences during mating season consortships. Relatedness did not influence partner choice on either alliance level. There is thus a striking resemblance between male dolphins, chimpanzees and humans, where closely bonded non-relatives engage in higher-level, polyadic cooperative acts. To that end, our study extends the scope of taxa in which social bonds rather than kinship explain cooperation, providing the first evidence that such traits might have evolved independently in marine and terrestrial realms.