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.

Reconstructing the colonization history of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Northwestern Australia.

Bottlenose dolphins (Tursiops spp.) are found in waters around Australia, with T. truncatus typically occupying deeper, more oceanic habitat, while T. aduncus occur in shallower, coastal waters. Little is known about the colonization history of T. aduncus along the Western Australian coastline; however, it has been hypothesized that extant populations are the result of an expansion along the coastline originating from a source in the north of Australia. To investigate the history of coastal T. aduncus populations in the area, we generated a genomic SNP dataset using a double-digest restriction-site-associated DNA (ddRAD) sequencing approach. The resulting dataset consisted of 103,201 biallelic SNPs for 112 individuals which were sampled from eleven coastal and two offshore sites between Shark Bay and Cygnet Bay, Western Australia. Our population genomic analyses showed a pattern consistent with the proposed source in the north with significant isolation by distance along the coastline, as well as a reduction in genomic diversity measures along the coastline with Shark Bay showing the most pronounced reduction. Our demographic analysis indicated that the expansion of T. aduncus along the coastline began around the last glacial maximum and progressed southwards with the Shark Bay population being founded only 13 kya. Our results are in line with coastal colonization histories inferred for Tursiops globally, highlighting the ability of delphinids to rapidly colonize novel coastal niches as habitat is released during glacial cycle-related global sea level and temperature changes.

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.

A stochastic model for estimating sustainable limits to wildlife mortality in a changing world.

Human-caused mortality of wildlife is a pervasive threat to biodiversity. Assessing the population-level impact of fisheries bycatch and other human-caused mortality of wildlife has typically relied upon deterministic methods. However, population declines are often accelerated by stochastic factors that are not accounted for in such conventional methods. Building on the widely applied potential biological removal (PBR) equation, we devised a new population modeling approach for estimating sustainable limits to human-caused mortality and applied it in a case study of bottlenose dolphins affected by capture in an Australian demersal otter trawl fishery. Our approach, termed sustainable anthropogenic mortality in stochastic environments (SAMSE), incorporates environmental and demographic stochasticity, including the dependency of offspring on their mothers. The SAMSE limit is the maximum number of individuals that can be removed without causing negative stochastic population growth. We calculated a PBR of 16.2 dolphins per year based on the best abundance estimate available. In contrast, the SAMSE model indicated that only 2.3-8.0 dolphins could be removed annually without causing a population decline in a stochastic environment. These results suggest that reported bycatch rates are unsustainable in the long term, unless reproductive rates are consistently higher than average. The difference between the deterministic PBR calculation and the SAMSE limits showed that deterministic approaches may underestimate the true impact of human-caused mortality of wildlife. This highlights the importance of integrating stochasticity when evaluating the impact of bycatch or other human-caused mortality on wildlife, such as hunting, lethal control measures, and wind turbine collisions. Although population viability analysis (PVA) has been used to evaluate the impact of human-caused mortality, SAMSE represents a novel PVA framework that incorporates stochasticity for estimating acceptable levels of human-caused mortality. It offers a broadly applicable, stochastic addition to the demographic toolbox to evaluate the impact of human-caused mortality on wildlife.

La mortalidad de la fauna causada por humanos es una amenaza continua para la biodiversidad. El análisis del impacto a nivel poblacional de la captura pesquera incidental y otras causas humanas de la mortalidad de la fauna comúnmente ha dependido de métodos determinísticos. Sin embargo, las declinaciones poblacionales con frecuencia se aceleran por los factores estocásticos que no son considerados en dichos métodos convencionales. A partir de la ecuación de extirpación biológica potencial (EBP) de extensa aplicación diseñamos una nueva estrategia de modelación poblacional para estimar los límites sustentables de la mortalidad causada por humanos y la aplicamos en un estudio de caso de los delfines nariz de botella afectados por la captura en una pesquería australiana de arrastre demersal. Nuestra estrategia, denominada mortalidad antropogénica sustentable en ambientes estocásticos (MASAM) incorpora la estocasticidad ambiental y demográfica, incluyendo la dependencia que tienen las crías por sus madres. El límite MASAM es el número máximo de individuos que pueden extirparse sin causar un crecimiento poblacional estocástico negativo. Calculamos un EBP de 16.3 delfines por año con base en la mejor estimación de abundancia disponible. Como contraste, el modelo MASAM indicó que sólo podían extirparse entre 2.3 y 8.0 delfines anualmente sin ocasionar una declinación poblacional en un ambiente estocástico. Estos resultados sugieren que las tasas reportadas de captura incidental no son sustentables a largo plazo, a menos que las tasas reproductivas sean sistemáticamente más altas que el promedio. La diferencia entre el cálculo determinístico del EBP y los límites de MASAM mostró que los enfoques determinísticos pueden subestimar el verdadero impacto de la mortalidad de la fauna causada por humanos. Lo anterior resalta la importancia de integrar la estocasticidad al evaluar el impacto de la captura incidental y otras causas humanas de la mortalidad como la caza, las medidas letales de control y las colisiones con turbinas de viento. Aunque el análisis de viabilidad poblacional (AVP) se ha utilizado para evaluar el impacto de la mortalidad causada por humanos, MASAM representa un marco novedoso de AVP que incorpora la estocasticidad para estimar los niveles aceptables de mortalidad causada por humanos. Este enfoque ofrece una adición estocástica de aplicación generalizada para las herramientas demográficas usadas para evaluar el impacto de la mortalidad causada por humanos sobre la fauna.

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.

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.

Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines.

Behavioural differences among social groups can arise from differing ecological conditions, genetic predispositions and/or social learning. In the past, social learning has typically been inferred as responsible for the spread of behaviour by the exclusion of ecological and genetic factors. This 'method of exclusion' was used to infer that 'sponging', a foraging behaviour involving tool use in the bottlenose dolphin (Tursiops aduncus) population in Shark Bay, Western Australia, was socially transmitted. However, previous studies were limited in that they never fully accounted for alternative factors, and that social learning, ecology and genetics are not mutually exclusive in causing behavioural variation. Here, we quantified the importance of social learning on the diffusion of sponging, for the first time explicitly accounting for ecological and genetic factors, using a multi-network version of 'network-based diffusion analysis'. Our results provide compelling support for previous findings that sponging is vertically socially transmitted from mother to (primarily female) offspring. This research illustrates the utility of social network analysis in elucidating the explanatory mechanisms behind the transmission of behaviour in wild animal populations.

Genetic isolation between coastal and fishery-impacted, offshore bottlenose dolphin (Tursiops spp.) populations.

The identification of species and population boundaries is important in both evolutionary and conservation biology. In recent years, new population genetic and computational methods for estimating population parameters and testing hypotheses in a quantitative manner have emerged. Using a Bayesian framework and a quantitative model-testing approach, we evaluated the species status and genetic connectedness of bottlenose dolphin (Tursiops spp.) populations off remote northwestern Australia, with a focus on pelagic 'offshore' dolphins subject to incidental capture in a trawl fishery. We analysed 71 dolphin samples from three sites beyond the 50 m depth contour (the inshore boundary of the fishery) and up to 170 km offshore, including incidentally caught and free-ranging individuals associating with trawl vessels, and 273 dolphins sampled at 12 coastal sites inshore of the 50 m depth contour and within 10 km of the coast. Results from 19 nuclear microsatellite markers showed significant population structure between dolphins from within the fishery and coastal sites, but also among dolphins from coastal sites, identifying three coastal populations. Moreover, we found no current or historic gene flow into the offshore population in the region of the fishery, indicating a complete lack of recruitment from coastal sites. Mitochondrial DNA corroborated our findings of genetic isolation between dolphins from the offshore population and coastal sites. Most offshore individuals formed a monophyletic clade with common bottlenose dolphins (T. truncatus), while all 273 individuals sampled coastally formed a well-supported clade of Indo-Pacific bottlenose dolphins (T. aduncus). By including a quantitative modelling approach, our study explicitly took evolutionary processes into account for informing the conservation and management of protected species. As such, it may serve as a template for other, similarly inaccessible study populations.

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.

Sexual Dimorphism and Geographic Variation in Dorsal Fin Features of Australian Humpback Dolphins, Sousa sahulensis.

Determining the sex of free-ranging cetaceans can be challenging. Sexual dimorphism among external features may allow inferences on sex, but such patterns may be difficult to detect and are often confounded by age and geographic variation. Dorsal fin images of 107 female and 54 male Australian humpback dolphins, Sousa sahulensis, from Western Australia (WA) and Queensland (QLD) were used to investigate sex, age and geographic differences in colouration, height/length quotient and number of notches. Adult males exhibited more dorsal fin notches (p<0.001) and a significantly greater loss of pigmentation on the upper half of their dorsal fins (p<0.001) than did adult females. These differences likely reflect that males experience a higher frequency and/or intensity of intraspecific aggression than females. In QLD, heavily spotted dorsal fins were more frequent among females than males (p<0.001). Logistic regression analyses revealed that dorsal fin spotting and loss of pigmentation on the upper half of the dorsal fin provided the best model parameters for predicting the sex of sampled adults, with 97% accuracy. This technique offers a rapid, non-invasive method for predicting sex in Australian humpback dolphins, which could potentially be applied to populations throughout their range. In contrast to adults, presumed immature animals showed little or no loss of pigmentation or spotting; however, the rate of development of these features remains unknown. There were pronounced differences between QLD and WA in the intensity of spotting on dorsal fins and the extent of pigmentation loss around the posterior insertion and trailing edge of the dorsal fin. While based on a limited sample size, these geographic differences may have conservation implications in terms of population subdivision and should be investigated further.

Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins.

Socially learned behaviours leading to genetic population structure have rarely been described outside humans. Here, we provide evidence of fine-scale genetic structure that has probably arisen based on socially transmitted behaviours in bottlenose dolphins (Tursiops sp.) in western Shark Bay, Western Australia. We argue that vertical social transmission in different habitats has led to significant geographical genetic structure of mitochondrial DNA (mtDNA) haplotypes. Dolphins with mtDNA haplotypes E or F are found predominantly in deep (more than 10 m) channel habitat, while dolphins with a third haplotype (H) are found predominantly in shallow habitat (less than 10 m), indicating a strong haplotype-habitat correlation. Some dolphins in the deep habitat engage in a foraging strategy using tools. These 'sponging' dolphins are members of one matriline, carrying haplotype E. This pattern is consistent with what had been demonstrated previously at another research site in Shark Bay, where vertical social transmission of sponging had been shown using multiple lines of evidence. Using an individual-based model, we found support that in western Shark Bay, socially transmitted specializations may have led to the observed genetic structure. The reported genetic structure appears to present an example of cultural hitchhiking of mtDNA haplotypes on socially transmitted foraging strategies, suggesting that, as in humans, genetic structure can be shaped through cultural transmission.

Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche.

Culturally transmitted tool use has important ecological and evolutionary consequences and has been proposed as a significant driver of human evolution. Such evidence is still scarce in other animals. In cetaceans, tool use has been inferred using indirect evidence in one population of Indo-Pacific bottlenose dolphins (Tursiops sp.), where particular dolphins ('spongers') use marine sponges during foraging. To date, evidence of whether this foraging tactic actually provides access to novel food items is lacking. We used fatty acid (FA) signature analysis to identify dietary differences between spongers and non-spongers, analysing data from 11 spongers and 27 non-spongers from two different study sites. Both univariate and multivariate analyses revealed significant differences in FA profiles between spongers and non-spongers between and within study sites. Moreover, FA profiles differed significantly between spongers and non-spongers foraging within the same deep channel habitat, whereas the profiles of non-spongers from deep channel and shallow habitats at this site could not be distinguished. Our results indicate that sponge use by bottlenose dolphins is linked to significant differences in diet. It appears that cultural transmission of tool use in dolphins, as in humans, allows the exploitation of an otherwise unused niche.

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'.

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.

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.

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.