Michael Krützen

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.

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.

'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 mothers 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.

Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins

Few studies of kinship in mammalian societies have been able to consider the complex interactions between home range overlap, association patterns and kinship, which have created a critical gap in our understanding of social evolution. We investigated the association patterns of female bottlenose dolphins, Tursiops aduncus, in the eastern gulf of Shark Bay, Western Australia and found that they depended upon the complex interplay of at least three factors: home range overlap, matrilineal kinship and biparental kinship. While home range overlap was positively correlated with female association patterns, preferred associations were found between females showing as little as 27% home range overlap, and some pairs showed avoidance despite 100% home range overlap. Furthermore, on average, both casual and preferred associations took place between females that were more closely biparentally related than expected by chance and this pattern varied depending upon whether or not pairs of females shared the same matriline.

Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus)

Sundaland, a tropical hotspot of biodiversity comprising Borneo and Sumatra among other islands, the Malay Peninsula, and a shallow sea, has been subject to dramatic environmental processes. Thus, it presents an ideal opportunity to investigate the role of environmental mechanisms in shaping species distribution and diversity. We investigated the population structure and underlying mechanisms of an insular endemic, the Bornean orangutan (Pongo pygmaeus). Phylogenetic reconstructions based on mtDNA sequences from 211 wild orangutans covering the entire range of the species indicate an unexpectedly recent common ancestor of Bornean orangutans 176 ka (95% highest posterior density, 72–322 ka), pointing to a Pleistocene refugium. High mtDNA differentiation among populations and rare haplotype sharing is consistent with a pattern of strong female philopatry. This is corroborated by isolation by distance tests, which show a significant correlation between mtDNA divergence and distance and a strong effect of rivers as barriers for female movement. Both frequency-based and Bayesian clustering analyses using as many as 25 nuclear microsatellite loci revealed a significant separation among all populations, as well as a small degree of male-mediated gene flow. This study highlights the unique effects of environmental and biological features on the evolutionary history of Bornean orangutans, a highly endangered species particularly vulnerable to future climate and anthropogenic change as an insular endemic.

Sex-Biased Dispersal and Volcanic Activities Shaped Phylogeographic Patterns of Extant Orangutans (genus: Pongo)

The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.

Integrating multiple lines of evidence to better understand the evolutionary divergence of humpback dolphins along their entire distribution range: a new dolphin species in Australian waters?

The conservation of humpback dolphins, distributed in coastal waters of the Indo‐West Pacific and eastern Atlantic Oceans, has been hindered by a lack of understanding about the number of species in the genus (Sousa) and their population structure. To address this issue, we present a combined analysis of genetic and morphologic data collected from beach‐cast, remote‐biopsied and museum specimens from throughout the known Sousa range. We extracted genetic sequence data from 235 samples from extant populations and explored the mitochondrial control region and four nuclear introns through phylogenetic, population‐level and population aggregation frameworks. In addition, 180 cranial specimens from the same geographical regions allowed comparisons of 24 morphological characters through multivariate analyses. The genetic and morphological data showed significant and concordant patterns of geographical segregation, which are typical for the kind of demographic isolation displayed by species units, across the Sousa genus distribution range. Based on our combined genetic and morphological analyses, there is convincing evidence for at least four species within the genus (S. teuszii in the Atlantic off West Africa, S. plumbea in the central and western Indian Ocean, S. chinensis in the eastern Indian and West Pacific Oceans, and a new as‐yet‐unnamed species off northern Australia).

Male dolphin alliances in Shark Bay: changing perspectives in a 30-year study

Bottlenose dolphins, Tursiops cf. aduncus, in Shark Bay, Western Australia exhibit the most complex alliances known outside of humans. Advances in our understanding of these alliances have occurred with expansions of our study area each decade. In the 1980s, we discovered that males cooperated in stable trios and pairs (first-order alliances) to herd individual oestrous females, and that two such alliances of four to six, sometimes related, individuals (second-order alliances) cooperated against other males in contests over females. The 1990s saw the discovery of a large 14-member second-order alliance whose members exhibited labile first-order alliance formation among nonrelatives. Partner preferences as well as a relationship between first-order alliance stability and consortship rate in this ‘super-alliance’ indicated differentiated relationships. The contrast between the super-alliance and the 1980s alliances suggested two alliance tactics. An expansion of the study area in the 2000s revealed a continuum of second-order alliance sizes in an open social network and no simple relationship between second-order alliance size and alliance stability, but generalized the relationship between first-order alliance stability and consortship rate within second-order alliances. Association preferences and contests involving three second-order alliances indicated the presence of third-order alliances. Second-order alliances may persist for 20 years with stability thwarted by gradual attrition, but underlying flexibility is indicated by observations of individuals joining other alliances, including old males joining young or old second-order alliances. The dolphin research has informed us on the evolution of complex social relationships and large brain evolution in mammals and the ecology of alliance formation. Variation in odontocete brain size and the large radiation of delphinids into a range of habitats holds great promise that further effort to describe their societies will be rewarded with similar advances in our understanding of these important issues.

Abundance, survival and temporary emigration of bottlenose dolphins (Tursiops sp.) off Useless Loop in the western gulf of Shark Bay, Western Australia

Capture–recapture models were used to provide estimates of abundance, apparent survival and temporary emigration of Indo-Pacific bottlenose dolphins (Tursiops sp.) in a 226-km2 study area off Useless Loop in the western gulf of Shark Bay, Western Australia. Photo-identification data were collected during boat-based surveys in Austral autumn to early spring (April–September) from 2007 to 2011. Abundance estimates varied from 115 (s.e. 5.2, 95% CI 105–126) individuals in 2008 to 208 (s.e. 17.3, 95% CI 177–245) individuals in 2010. The variability in abundance estimates is likely to be a reflection of how individuals used the study area, rather than fluctuations in true population size. The best fitting capture–recapture model suggested a random temporary emigration pattern and, when coupled with relatively high temporary emigration rates (0.33 (s.e. 0.07) – 0.66 (s.e. 0.05)) indicated that the study area did not cover the entire ranges of the photo-identified dolphins. Apparent survival rate is a product of true survival and permanent emigration and was estimated annually at 0.95 (s.e. 0.02). Since permanent emigration from the study area is unlikely, true survival was estimated to be close to 0.95. This study provides a robust baseline for future comparisons of dolphin demographics, which may be of importance should climate change or increasing anthropogenic activity affect this population.