Luciana M. Möller

Genetic evidence for sex‐biased dispersal in resident bottlenose dolphins (Tursiops aduncus)

In most mammals males usually disperse before breeding, while females remain in their natal group or area. However, in odontocete cetaceans behavioural and/or genetic evidence from populations of four species indicate that both males and females remain in their natal group or site. For coastal resident bottlenose dolphins field data suggest that both sexes are philopatric to their natal site. Assignment tests and analyses of relatedness based on microsatellite markers were used to investigate this hypothesis in resident bottlenose dolphins, Tursiops aduncus, from two small coastal populations of southeastern Australia. Mean corrected assignment and mean relatedness were higher for resident females than for resident males. Only 8% of resident females had a lower probability than average of being born locally compared to 33% of resident males. Our genetic data contradict the hypothesis of bisexual philopatry to natal site and suggest that these bottlenose dolphins are not unusual amongst mammals, with females being the more philopatric and males the more dispersing sex.

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.

Social cohesion in a hierarchically structured embayment population of Indo-Pacific bottlenose dolphins

We investigated community structure and association patterns for a small population of Indo-Pacific bottlenose dolphins, Tursiops aduncus, inhabiting the Port Stephens embayment in southeastern Australia. Association data for 120 regularly sighted individuals were obtained from seasonal photoidentification surveys collected over 7 years (1998–2007). Using a combined cluster and social network analysis approach, we found association patterns between dolphins were hierarchically structured, where two mixed-sex communities were subdivided into smaller, temporarily dynamic social groups. Community membership corresponded to differences in individual ranging patterns and habitat occupation. The larger eastern community inhabits a typically marine environment, while individuals of the western community range over a larger area that is dominated by estuarine processes. Both communities were composed of long-term preferred companions; however, the degree of social cohesion differed considerably between the two communities. Associations between individuals were considerably stronger and temporally more stable in the western community. Western individuals also had significantly fewer preferred associates despite living in similar-sized schools. Finally, in direct contrast to associations within each community, intercommunity associations were highly variable and resulted primarily from aggregative behaviour. We propose the segregation of communities resulted from individual adaptation to local environmental conditions, facilitated by individual variability in association preferences. The disparity in association patterns between communities may have resulted from a combination of ecological, population density, kinship and anthropogenic factors.

Association patterns and kinship in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Kinship has been shown to be an important correlate of group membership and associations among many female mammals. In this study, we investigate association patterns in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting an embayment in southeastern Australia. We combine the behavioral data with microsatellite DNA and mitochondrial DNA data to test the hypotheses that genetic relatedness and maternal kinship correlate with associations and social clusters. Mean association between females was not significantly different from a random mean, but the standard deviation was significantly higher than a random standard deviation, indicating the presence of nonrandom associates in the dataset. A neighbor-joining tree, based on the distance of associations between females, identified four main social clusters in the area. Mean genetic relatedness between pairs of frequent female associates was significantly higher than that between pairs of infrequent associates. There was also a significant correlation between mtDNA haplotype sharing and the degree of female association. However, the mean genetic relatedness of female pairs within and between social clusters and the proportion of female pairs with the same and different mtDNA haplotypes within and between clusters were not significantly different. This study demonstrates that kinship correlates with associations among female bottlenose dolphins, but that kinship relations are not necessarily a prerequisite for membership in social clusters. We hypothesize that different forces acting on female bottlenose dolphin sociality appear to promote the formation of flexible groups which include both kin and nonkin.

Habitat type promotes rapid and extremely localised genetic differentiation in dolphins

The high potential for dispersal of many marine organisms often results in low population differentiation over large distances. Here, we report that dolphin communities living in very close geographic proximity (<16 km) but in two different environments – open coast and enclosed embayment – exhibit unexpected genetic differentiation at nine microsatellite loci. Results based on a fixation index and a Bayesian clustering approach suggested that gene flow between communities within an embayment is high, as is gene flow between coastal communities. However, lower gene flow between embayment and open coast communities translated into substantial genetic differentiation between dolphin communities from the two environments, and assignment of individuals into two populations. Along with patterns observed in 403 bp of the mitochondrial DNA control region, the results suggest that restriction of gene flow likely occurred in the last 6000 years, after coastal dolphins colonised the embayment. We hypothesise that factors such as fidelity to the local area and resource and behavioural specialisations may have played a major role in promoting and maintaining genetic subdivision between dolphins of the two environments. Importantly, our study shows that habitat type can rapidly promote extremely fine-scale genetic structure in a long-lived, highly mobile marine mammal.

Female bisexual kinship ties maintain social cohesion in a dolphin network

Social assortativity, where individuals preferentially mix with certain conspecifics, is widespread among a diverse range of taxa. Animals may assort by a variety of characteristics and receive substantial benefits from these interactions, such as a reduction in predation risk, increased foraging efficiency or greater access to resources. We investigated the social network structure of an embayment population of Indo-Pacific bottlenose dolphins, Tursiops aduncus, using a long-term photoidentification data set, and examined the impact of sex and kinship in maintaining the cohesion of the social network. We applied recently developed social network techniques that incorporate uncertainty into statistical measures to delineate four smaller social groups within two previously defined communities. Temporal stability of associations within social groups was substantially greater than among individuals from different groups. We also found that the dolphin population was not strongly segregated by sex and both males and females had similar degrees of social connectivity in the network. Moreover, genetic analyses showed that relatedness had a greater influence on female than on male social relationships, as association strength was positively correlated with genetic relatedness between females and between female and male pairs, but not between males. These results suggest that females and males may target kin interactions with females and that kinship appears to be important for maintaining the cohesiveness of this dolphin social network.

Multi-gene evidence for a new bottlenose dolphin species in southern Australia

Marine Mammal Research Group, Graduate School of the Environment, Macquarie University, Sydney, NSW 2109, Australia Molecular Ecology Lab, Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia Centre for Environmental Stress and Adaptation Research (CESAR) and Australian Centre for Biodiversity: Analysis, Policy and Management, School of Biological Sciences, Monash University, VIC. 3800, Australia

Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in Southeastern Australia

Determining genetic connectivity of bottlenose dolphin communities helps identify evolutionary mechanisms, such as environmental and social factors, that interact to shape dispersal in highly social marine mammals. Here, we expand on a localized study that found marked genetic differentiation among resident dolphins (Tursiops aduncus) in the Port Stephens embayment and adjacent coastal communities, to include four additional communities inhabiting different environment types along the New South Wales coast, Southeastern Australia. Analysis of the mitochondrial DNA control region and seven microsatellite loci suggest the nine communities may have originated from a single ancestral population that progressively colonised the coast in a southward direction. Gene flow among communities was predominately governed by habitat type. The two enclosed embayments showed the highest level of genetic differentiation from other communities, while genetic differentiation among coastal and open embayment communities generally followed a pattern of isolation by distance. Directional bias in recent migration rates was evident, with the centrally located Hunter coast communities consisting of individuals with mixed ancestry from the Northern, Southern and Port Stephens communities. Emigration from Port Stephens was substantially higher than in the opposite direction, indicating there may be social barriers to dispersal created by Port Stephens dolphins. Our results suggest that the scale of connectivity of bottlenose dolphin communities inhabiting heterogeneous environments is likely to be affected by local habitat adaptation. This has important implications for the management of communities exposed to increasing levels of anthropogenic disturbances, such as the intensive commercial dolphin-watching industry operating in Port Stephens.

Sociogenetic structure, kin associations and bonding in delphinids

Social systems are the outcomes of natural and sexual selection on individuals’ efforts to maximize reproductive success. Ecological conditions, life history, demography traits and social aspects have been recognized as important factors shaping social systems. Delphinids show a wide range of social structures and large variation in life history traits and inhabit several aquatic environments. They are therefore an excellent group in which to investigate the interplay of ecological and intrinsic factors on the evolution of mammalian social systems in these environments. Here I synthetize results from genetic studies on dispersal patterns, genetic relatedness, kin associations and mating patterns and combine with ecological, life history and phylogenetic data to predict the formation of kin associations and bonding in these animals. I show that environment type impacts upon dispersal tendencies, with small delphinids generally exhibiting female‐biased philopatry in inshore waters and bisexual dispersal in coastal and pelagic waters. When female philopatry occurs, they develop moderate social bonds with related females. Male bonding occurs in species with small male‐biased sexual size dimorphism and male‐biased operational sex ratio, and it is independent of dispersal tendencies. By contrast, large delphinids, which live in coastal and pelagic waters, show bisexual philopatry and live in matrilineal societies. I propose that sexual conflict favoured the formation of these stable societies and in turn facilitated the development of kin‐biased behaviours. Studies on populations of the same species inhabiting disparate environments, and of less related species living in similar habitats, would contribute towards a comprehensive framework for the evolution of delphinid social systems.

Recent Diversification of a Marine Genus (Tursiops spp.) Tracks Habitat Preference and Environmental Change

Understanding the evolution of diversity and the resulting systematics in marine systems is confounded by the lack of clear boundaries in oceanic habitats, especially for highly mobile species like marine mammals. Dolphin populations and sibling species often show differentiation between coastal and offshore habitats, similar to the pelagic/littoral or benthic differentiation seen for some species of fish. Here we test the hypothesis that lineages within the polytypic genus Tursiops track past changes in the environment reflecting ecological drivers of evolution facilitated by habitat release. We used a known recent time point for calibration (the opening of the Bosphorus) and whole mitochondrial genome (mitogenome) sequences for high phylogenetic resolution. The pattern of lineage formation suggested an origin in Australasia and several early divisions involving forms currently inhabiting coastal habitats. Radiation in pelagic environments was relatively recent, and was likely followed by a return to coastal habitat in some regions. The timing of some nodes defining different ecotypes within the genus clustered near the two most recent interglacial transitions. A signal for an increase in diversification was also seen for dates after the last glacial maximum. Together these data suggest the tracking of habitat preference during geographic expansions, followed by transition points reflecting habitat shifts, which were likely associated with periods of environmental change.