Genomic Divergence and the Evolution of Ecotypes in Bottlenose Dolphins (Genus Tursiops).

Climatic changes have caused major environmental restructuring throughout the world's oceans. Marine organisms have responded to novel conditions through various biological systems, including genomic adaptation. Growing accessibility of next-generation DNA sequencing methods to study nonmodel species has recently allowed genomic changes underlying environmental adaptations to be investigated. This study used double-digest restriction-site associated DNA (ddRAD) sequence data to investigate the genomic basis of ecotype formation across currently recognized species and subspecies of bottlenose dolphins (genus Tursiops) in the Southern Hemisphere. Subspecies-level genomic divergence was confirmed between the offshore common bottlenose dolphin (T. truncatus truncatus) and the inshore Lahille's bottlenose dolphin (T. t. gephyreus) from the southwestern Atlantic Ocean (SWAO). Similarly, subspecies-level divergence is suggested between inshore (eastern Australia) Indo-Pacific bottlenose dolphin (T. aduncus) and the proposed Burrunan dolphin (T. australis) from southern Australia. Inshore bottlenose dolphin lineages generally had lower genomic diversity than offshore lineages, a pattern particularly evident for T. t. gephyreus, which showed exceptionally low diversity. Genomic regions associated with cardiovascular, musculoskeletal, and energy production systems appear to have undergone repeated adaptive evolution in inshore lineages across the Southern Hemisphere. We hypothesize that comparable selective pressures in the inshore environment drove similar adaptive responses in each lineage, supporting parallel evolution of inshore bottlenose dolphins. With climate change altering marine ecosystems worldwide, it is crucial to gain an understanding of the adaptive capacity of local species and populations. Our study provides insights into key adaptive pathways that may be important for the long-term survival of cetaceans and other organisms in a changing marine environment.

Seascape genomics of common dolphins (Delphinus delphis) reveals adaptive diversity linked to regional and local oceanography.

BACKGROUND: High levels of standing genomic variation in wide-ranging marine species may enhance prospects for their long-term persistence. Patterns of connectivity and adaptation in such species are often thought to be influenced by spatial factors, environmental heterogeneity, and oceanographic and geomorphological features. Population-level studies that analytically integrate genome-wide data with environmental information (i.e., seascape genomics) have the potential to inform the spatial distribution of adaptive diversity in wide-ranging marine species, such as many marine mammals. We assessed genotype-environment associations (GEAs) in 214 common dolphins (Delphinus delphis) along > 3000 km of the southern coast of Australia. RESULTS: We identified 747 candidate adaptive SNPs out of a filtered panel of 17,327 SNPs, and five putatively locally-adapted populations with high levels of standing genomic variation were disclosed along environmentally heterogeneous coasts. Current velocity, sea surface temperature, salinity, and primary productivity were the key environmental variables associated with genomic variation. These environmental variables are in turn related to three main oceanographic phenomena that are likely affecting the dispersal of common dolphins: (1) regional oceanographic circulation, (2) localised and seasonal upwellings, and (3) seasonal on-shelf circulation in protected coastal habitats. Signals of selection at exonic gene regions suggest that adaptive divergence is related to important metabolic traits. CONCLUSION: To the best of our knowledge, this represents the first seascape genomics study for common dolphins (genus Delphinus). Information from the associations between populations and their environment can assist population management in forecasting the adaptive capacity of common dolphins to climate change and other anthropogenic impacts.

Seascape genomics of coastal bottlenose dolphins along strong gradients of temperature and salinity.

Heterogeneous seascapes and strong environmental gradients in coastal waters are expected to influence adaptive divergence, particularly in species with large population sizes where selection is expected to be highly efficient. However, these influences might also extend to species characterized by strong social structure, natal philopatry and small home ranges. We implemented a seascape genomic study to test this hypothesis in Indo-Pacific bottlenose dolphins (Tursiops aduncus) distributed along the environmentally heterogeneous coast of southern Australia. The data sets included oceanographic and environmental variables thought to be good predictors of local adaptation in dolphins and 8081 filtered single nucleotide polymorphisms (SNPs) genotyped for individuals sampled from seven different bioregions. From a neutral perspective, population structure and connectivity of the dolphins were generally influenced by habitat type and social structuring. Genotype-environment association analysis identified 241 candidate adaptive loci and revealed that sea surface temperature and salinity gradients influenced adaptive divergence in these animals at both large- (1000 km) and fine-scales (<100 km). Enrichment analysis and annotation of candidate genes revealed functions related to sodium-activated ion transport, kidney development, adipogenesis and thermogenesis. The findings of spatial adaptive divergence and inferences of putative physiological adaptations challenge previous suggestions that marine megafauna is most likely to be affected by environmental and climatic changes via indirect, trophic effects. Our work contributes to conservation management of coastal bottlenose dolphins subjected to anthropogenic disturbance and to efforts of clarifying how seascape heterogeneity influences adaptive diversity and evolution in small cetaceans.

Longitudinal monitoring of neutral and adaptive genomic diversity in a reintroduction.

Restoration programs in the form of ex-situ breeding combined with reintroductions are becoming critical to counteract demographic declines and species losses. Such programs are increasingly using genetic management to improve conservation outcomes. However, the lack of long-term monitoring of genetic indicators following reintroduction prevents assessments of the trajectory and persistence of reintroduced populations. We carried out an extensive monitoring program in the wild for a threatened small-bodied fish (southern pygmy perch, Nannoperca australis) to assess the long-term genomic effects of its captive breeding and reintroduction. The species was rescued prior to its extirpation from the terminal lakes of Australia's Murray-Darling Basin, and then used for genetically informed captive breeding and reintroductions. Subsequent annual or biannual monitoring of abundance, fitness, and occupancy over a period of 11 years, combined with postreintroduction genetic sampling, revealed survival and recruitment of reintroduced fish. Genomic analyses based on data from the original wild rescued, captive born, and reintroduced cohorts revealed low inbreeding and strong maintenance of neutral and candidate adaptive genomic diversity across multiple generations. An increasing trend in the effective population size of the reintroduced population was consistent with field monitoring data in demonstrating successful re-establishment of the species. This provides a rare empirical example that the adaptive potential of a locally extinct population can be maintained during genetically informed ex-situ conservation breeding and reintroduction into the wild. Strategies to improve biodiversity restoration via ex-situ conservation should include genetic-based captive breeding and longitudinal monitoring of standing genomic variation in reintroduced populations.

Monitoreo Longitudinal de la Diversidad Genómica Neutral y Adaptativa en una Reintroducción Marshall et al. 21-643 Resumen Los programas de restauración a manera de reproducción ex situ combinada con reintroducciones se están volviendo críticos para contrarrestar las declinaciones demográficas y la pérdida de especies. Dichos programas usan cada vez más la gestión genética para mejorar los resultados de conservación. Sin embargo, la falta de monitoreo a largo plazo de los indicadores genéticos posteriores a la reintroducción evita que se realicen evaluaciones de la trayectoria y la persistencia de las poblaciones reintroducidas. Se rescató un pez de talla pequeña (percha pigmea del sur [Nannoperca australis]) previo a su extirpación de los lagos terminales de la Cuenca Murray-Darling en Australia para después reproducirlo en cautiverio con información genética y reintroducirlo. Realizamos monitoreos anuales o bianuales de la abundancia, aptitud y ocupación en vida silvestre durante once años, además de un muestreo genético posterior a la reintroducción. Analizamos los datos genómicos de los grupos originales rescatados, los nacidos en cautiverio y los reintroducidos. Nuestro objetivo era evaluar los efectos genómicos a largo plazo de la reproducción en cautiverio y la reintroducción de esta especie. Esto reveló baja endogamia y el sólido mantenimiento de la diversidad genómica neutral y adaptativa durante varias generaciones. Encontramos una coherencia entre la tendencia creciente en el tamaño de la población efectiva de la población reintroducida y los datos de campo que demostraron el restablecimiento exitoso de la especie. Nuestro estudio proporciona un raro ejemplo empírico de cómo el potencial adaptativo de una población localmente extinta puede mantenerse durante la reproducción de conservación ex situ genéticamente informada y su reintroducción. Las estrategias para mejorar la restauración de la biodiversidad por medio de la conservación ex situ deberían incluir la reproducción en cautiverio basada en la genética y el monitoreo longitudinal de la variación genómica actual de las poblaciones reintroducidas.

Whole genomes reveal multiple candidate genes and pathways involved in the immune response of dolphins to a highly infectious virus.

Wildlife species are challenged by various infectious diseases that act as important demographic drivers of populations and have become a great conservation concern particularly under growing environmental changes. The new era of whole genome sequencing provides new opportunities and avenues to explore the role of genetic variants in the plasticity of immune responses, particularly in non-model systems. Cetacean morbillivirus (CeMV) has emerged as a major viral threat to cetacean populations worldwide, contributing to the death of thousands of individuals of multiple dolphin and whale species. To understand the genomic basis of immune responses to CeMV, we generated and analysed whole genomes of 53 Indo-Pacific bottlenose dolphins (Tursiops aduncus) exposed to Australia's largest known CeMV-related mortality event that killed at least 50 dolphins from three different species. The genomic data set consisted of 10,168,981 SNPs anchored onto 23 chromosome-length scaffolds and 77 short scaffolds. Whole genome analysis indicated that levels of inbreeding in the dolphin population did not influence the outcome of an individual. Allele frequency estimates between survivors and nonsurvivors of the outbreak revealed 15,769 candidate SNPs, of which 689 were annotated to 295 protein coding genes. These included 50 genes with functions related to innate and adaptive immune responses, and cytokine signalling pathways and genes thought to be involved in immune responses to other morbilliviruses. Our study characterised genomic regions and pathways that may contribute to CeMV immune responses in dolphins. This represents a stride towards clarifying the complex interactions of the cetacean immune system and emphasises the value of whole genome data sets in understanding genetic elements that are essential for species conservation, including disease susceptibility and adaptation.

Abundance estimates and habitat preferences of bottlenose dolphins reveal the importance of two gulfs in South Australia.

Informed conservation management of marine mammals requires an understanding of population size and habitat preferences. In Australia, such data are needed for the assessment and mitigation of anthropogenic impacts, including fisheries interactions, coastal zone developments, oil and gas exploration and mining activities. Here, we present large-scale estimates of abundance, density and habitat preferences of southern Australian bottlenose dolphins (Tursiops sp.) over an area of 42,438km2 within two gulfs of South Australia. Using double-observer platform aerial surveys over four strata and mark-recapture distance sampling analyses, we estimated 3,493 (CV = 0.21; 95%CI = 2,327-5,244) dolphins in summer/autumn, and 3,213 (CV = 0.20; 95%CI = 2,151-4,801) in winter/spring of 2011. Bottlenose dolphin abundance and density was higher in gulf waters across both seasons (0.09-0.24 dolphins/km2) compared to adjacent shelf waters (0.004-0.04 dolphins/km2). The high densities of bottlenose dolphins in the two gulfs highlight the importance of these gulfs as a habitat for the species. Habitat modelling associated bottlenose dolphins with shallow waters, flat seafloor topography, and higher sea surface temperatures (SSTs) in summer/autumn and lower SSTs in winter/spring. Spatial predictions showed high dolphin densities in northern and coastal gulf sections. Distributional data should inform management strategies, marine park planning and environmental assessments of potential anthropogenic threats to this protected species.

Genome-wide association study of an unusual dolphin mortality event reveals candidate genes for susceptibility and resistance to cetacean morbillivirus.

Infectious diseases are significant demographic and evolutionary drivers of populations, but studies about the genetic basis of disease resistance and susceptibility are scarce in wildlife populations. Cetacean morbillivirus (CeMV) is a highly contagious disease that is increasing in both geographic distribution and incidence, causing unusual mortality events (UME) and killing tens of thousands of individuals across multiple cetacean species worldwide since the late 1980s. The largest CeMV outbreak in the Southern Hemisphere reported to date occurred in Australia in 2013, where it was a major factor in a UME, killing mainly young Indo-Pacific bottlenose dolphins (Tursiops aduncus). Using cases (nonsurvivors) and controls (putative survivors) from the most affected population, we carried out a genome-wide association study to identify candidate genes for resistance and susceptibility to CeMV. The genomic data set consisted of 278,147,988 sequence reads and 35,493 high-quality SNPs genotyped across 38 individuals. Association analyses found highly significant differences in allele and genotype frequencies among cases and controls at 65 SNPs, and Random Forests conservatively identified eight as candidates. Annotation of these SNPs identified five candidate genes (MAPK8, FBXW11, INADL, ANK3 and ACOX3) with functions associated with stress, pain and immune responses. Our findings provide the first insights into the genetic basis of host defence to this highly contagious disease, enabling the development of an applied evolutionary framework to monitor CeMV resistance across cetacean species. Biomarkers could now be established to assess potential risk factors associated with these genes in other CeMV-affected cetacean populations and species. These results could also possibly aid in the advancement of vaccines against morbilliviruses.

Modelling Dolphin Distribution to Inform Future Spatial Conservation Decisions in a Marine Protected Area.

As marine predators experience increasing anthropogenic pressures, there is an urgent need to understand their distribution and their drivers to inform spatial conservation planning. We used an ensemble modelling approach to investigate the spatio-temporal distribution of southern Australian bottlenose dolphins (Tursiops cf. australis) in relation to a variety of ecogeographical and anthropogenic variables in Coffin Bay, Thorny Passage Marine Park, South Australia. Further, we evaluated the overlap between current spatial management measures and important dolphin habitat. Dolphins showed no distinct seasonal shifts in distribution patterns. Models of the entire study area indicate that zones of high probability of dolphin occurrence were located mainly within the inner area of Coffin Bay. In the inner area, zones with high probability of dolphin occurrence were associated with shallow waters (2-4 m and 7-10 m) and located within 1,000 m from land and 2,500 m from oyster farms. The multi-modal response curve of depth in the models likely shows how the different dolphin communities in Coffin Bay occupy different embayments characterized by distinct depth patterns. The majority of areas of high (>0.6) probability of dolphin occurrence are outside sanctuary zones where multiple human activities are allowed. The inner area of Coffin Bay is an important area of year-round habitat suitability for dolphins. Our results can inform future spatial conservation decisions and improve protection of important dolphin habitat.

From conservation genetics to conservation genomics: a genome-wide assessment of blue whales (Balaenoptera musculus) in Australian feeding aggregations.

Genetic datasets of tens of markers have been superseded through next-generation sequencing technology with genome-wide datasets of thousands of markers. Genomic datasets improve our power to detect low population structure and identify adaptive divergence. The increased population-level knowledge can inform the conservation management of endangered species, such as the blue whale (Balaenoptera musculus). In Australia, there are two known feeding aggregations of the pygmy blue whale (B. m. brevicauda) which have shown no evidence of genetic structure based on a small dataset of 10 microsatellites and mtDNA. Here, we develop and implement a high-resolution dataset of 8294 genome-wide filtered single nucleotide polymorphisms, the first of its kind for blue whales. We use these data to assess whether the Australian feeding aggregations constitute one population and to test for the first time whether there is adaptive divergence between the feeding aggregations. We found no evidence of neutral population structure and negligible evidence of adaptive divergence. We propose that individuals likely travel widely between feeding areas and to breeding areas, which would require them to be adapted to a wide range of environmental conditions. This has important implications for their conservation as this blue whale population is likely vulnerable to a range of anthropogenic threats both off Australia and elsewhere.

Spatiotemporal use predicts social partitioning of bottlenose dolphins with strong home range overlap.

Ranging behaviour and temporal patterns of individuals are known to be fundamental sources of variation in social networks. Spatiotemporal dynamics can both provide and inhibit opportunities for individuals to associate, and should therefore be considered in social analysis. This study investigated the social structure of a Lahille's bottlenose dolphin (Tursiops truncatus gephyreus) population, which shows different spatiotemporal patterns of use and gregariousness between individuals. For this, we constructed an initial social network using association indices corrected for gregariousness and then uncovered affiliations from this social network using generalized affiliation indices. The association-based social network strongly supported that this dolphin population consists of four social units highly correlated to spatiotemporal use patterns. Excluding the effects of gregariousness and spatiotemporal patterns, the affiliation-based social network suggested an additional two social units. Although the affiliation-based social units shared a large part of their core areas, space and/or time use by individuals of the different units were generally distinct. Four of the units were strongly associated with both estuarine and shallow coastal areas, while the other two units were restricted to shallow coastal waters to the south (SC) and north of the estuary (NC), respectively. Interactions between individuals of different social units also occurred, but dolphins from the NC were relatively more isolated and mainly connected to SC dolphins. From a conservation management perspective, it is recommended that information about the dolphin social units should be incorporated in modeling intrapopulation dynamics and viability, as well as for investigating patterns of gene flow among them.

Genotyping-by-sequencing for estimating relatedness in nonmodel organisms: Avoiding the trap of precise bias.

There has been remarkably little attention to using the high resolution provided by genotyping-by-sequencing (i.e., RADseq and similar methods) for assessing relatedness in wildlife populations. A major hurdle is the genotyping error, especially allelic dropout, often found in this type of data that could lead to downward-biased, yet precise, estimates of relatedness. Here, we assess the applicability of genotyping-by-sequencing for relatedness inferences given its relatively high genotyping error rate. Individuals of known relatedness were simulated under genotyping error, allelic dropout and missing data scenarios based on an empirical ddRAD data set, and their true relatedness was compared to that estimated by seven relatedness estimators. We found that an estimator chosen through such analyses can circumvent the influence of genotyping error, with the estimator of Ritland (Genetics Research, 67, 175) shown to be unaffected by allelic dropout and to be the most accurate when there is genotyping error. We also found that the choice of estimator should not rely solely on the strength of correlation between estimated and true relatedness as a strong correlation does not necessarily mean estimates are close to true relatedness. We also demonstrated how even a large SNP data set with genotyping error (allelic dropout or otherwise) or missing data still performs better than a perfectly genotyped microsatellite data set of tens of markers. The simulation-based approach used here can be easily implemented by others on their own genotyping-by-sequencing data sets to confirm the most appropriate and powerful estimator for their data.

Genetic divergence between two phenotypically distinct bottlenose dolphin ecotypes suggests separate evolutionary trajectories.

Due to their worldwide distribution and occupancy of different types of environments, bottlenose dolphins display considerable morphological variation. Despite limited understanding about the taxonomic identity of such forms and connectivity among them at global scale, coastal (or inshore) and offshore (or oceanic) ecotypes have been widely recognized in several ocean regions. In the Southwest Atlantic Ocean (SWA), however, there are scarce records of bottlenose dolphins differing in external morphology according to habitat preferences that resemble the coastal-offshore pattern observed elsewhere. The main aim of this study was to analyze the genetic variability, and test for population structure between coastal (n = 127) and offshore (n = 45) bottlenose dolphins sampled in the SWA to assess whether their external morphological distinction is consistent with genetic differentiation. We used a combination of mtDNA control region sequences and microsatellite genotypes to infer population structure and levels of genetic diversity. Our results from both molecular marker types were congruent and revealed strong levels of structuring (microsatellites FST = 0.385, p < .001; mtDNA FST =  0.183, p < .001; ΦST = 0.385, p < .001) and much lower genetic diversity in the coastal than the offshore ecotype, supporting patterns found in previous studies elsewhere. Despite the opportunity for gene flow in potential "contact zones", we found minimal current and historical connectivity between ecotypes, suggesting they are following discrete evolutionary trajectories. Based on our molecular findings, which seem to be consistent with morphological differentiations recently described for bottlenose dolphins in our study area, we recommend recognizing the offshore bottlenose dolphin ecotype as an additional Evolutionarily Significant Unit (ESU) in the SWA. Implications of these results for the conservation of bottlenose dolphins in SWA are also discussed.

swinger: a user-friendly computer program to establish captive breeding groups that minimize relatedness without pedigree information.

Captive breeding programmes are often a necessity for the continued persistence of a population or species. They typically have the goal of maintaining genetic diversity and minimizing inbreeding. However, most captive breeding programmes have been based on the assumption that the founding breeders are unrelated and outbred, even though in situ anthropogenic impacts often mean these founders may have high relatedness and substantial inbreeding. In addition, polygamous group-breeding species in captivity often have uncertain pedigrees, making it difficult to select the group composition for subsequent breeding. Molecular-based estimates of relatedness and inbreeding may instead be used to select breeding groups (≥two individuals) that minimize relatedness and filter out inbred individuals. swinger constructs breeding groups based on molecular estimates of relatedness and inbreeding. The number of possible combinations of breeding groups quickly becomes intractable by hand. swinger was designed to overcome this major issue in ex situ conservation biology. The user can specify parameters within swinger to reach breeding solutions that suit the mating system of the target species and available resources. We provide evidence of the efficiency of the software with an empirical example and using simulations. The only data required are a typical molecular marker data set, such as a microsatellite or SNP data set, from which estimates of inbreeding and pairwise relatedness may be obtained. Such molecular data sets are becoming easier to gather from non-model organisms with next-generation sequencing technology. swinger is an open-source software with a user-friendly interface and is available at http://www.molecularecology.flinders.edu.au/molecular-ecology-lab/software/swinger/swinger/ and https://github.com/Yuma248/Swinger.

Towards population-level conservation in the critically endangered Antarctic blue whale: the number and distribution of their populations.

Population-level conservation is required to prevent biodiversity loss within a species, but it first necessitates determining the number and distribution of populations. Many whale populations are still depleted due to 20th century whaling. Whales are one of the most logistically difficult and expensive animals to study because of their mobility, pelagic lifestyle and often remote habitat. We tackle the question of population structure in the Antarctic blue whale (Balaenoptera musculus intermedia) - a critically endangered subspecies and the largest extant animal - by capitalizing on the largest genetic dataset to date for Antarctic blue whales. We found evidence of three populations that are sympatric in the Antarctic feeding grounds and likely occupy separate breeding grounds. Our study adds to knowledge of population structure in the Antarctic blue whale. Future research should invest in locating the breeding grounds and migratory routes of Antarctic blue whales through satellite telemetry to confirm their population structure and allow population-level conservation.

Low genetic diversity in pygmy blue whales is due to climate-induced diversification rather than anthropogenic impacts.

Unusually low genetic diversity can be a warning of an urgent need to mitigate causative anthropogenic activities. However, current low levels of genetic diversity in a population could also be due to natural historical events, including recent evolutionary divergence, or long-term persistence at a small population size. Here, we determine whether the relatively low genetic diversity of pygmy blue whales (Balaenoptera musculus brevicauda) in Australia is due to natural causes or overexploitation. We apply recently developed analytical approaches in the largest genetic dataset ever compiled to study blue whales (297 samples collected after whaling and representing lineages from Australia, Antarctica and Chile). We find that low levels of genetic diversity in Australia are due to a natural founder event from Antarctic blue whales (Balaenoptera musculus intermedia) that occurred around the Last Glacial Maximum, followed by evolutionary divergence. Historical climate change has therefore driven the evolution of blue whales into genetically, phenotypically and behaviourally distinct lineages that will likely be influenced by future climate change.

Hybridization of Southern Hemisphere blue whale subspecies and a sympatric area off Antarctica: impacts of whaling or climate change?

Understanding the degree of genetic exchange between subspecies and populations is vital for the appropriate management of endangered species. Blue whales (Balaenoptera musculus) have two recognized Southern Hemisphere subspecies that show differences in geographic distribution, morphology, vocalizations and genetics. During the austral summer feeding season, the Antarctic blue whale (B. m. intermedia) is found in polar waters and the pygmy blue whale (B. m. brevicauda) in temperate waters. Here, we genetically analyzed samples collected during the feeding season to report on several cases of hybridization between the two recognized blue whale Southern Hemisphere subspecies in a previously unconfirmed sympatric area off Antarctica. This means the pygmy blue whales using waters off Antarctica may migrate and then breed during the austral winter with the Antarctic subspecies. Alternatively, the subspecies may interbreed off Antarctica outside the expected austral winter breeding season. The genetically estimated recent migration rates from the pygmy to Antarctic subspecies were greater than estimates of evolutionary migration rates and previous estimates based on morphology of whaling catches. This discrepancy may be due to differences in the methods or an increase in the proportion of pygmy blue whales off Antarctica within the last four decades. Potential causes for the latter are whaling, anthropogenic climate change or a combination of these and may have led to hybridization between the subspecies. Our findings challenge the current knowledge about the breeding behaviour of the world's largest animal and provide key information that can be incorporated into management and conservation practices for this endangered species.

Influences of past climatic changes on historical population structure and demography of a cosmopolitan marine predator, the common dolphin (genus Delphinus).

Climatic oscillations during the Pleistocene have greatly influenced the distribution and connectivity of many organisms, leading to extinctions but also generating biodiversity. While the effects of such changes have been extensively studied in the terrestrial environment, studies focusing on the marine realm are still scarce. Here we used sequence data from one mitochondrial and five nuclear loci to assess the potential influence of Pleistocene climatic changes on the phylogeography and demographic history of a cosmopolitan marine predator, the common dolphin (genus Delphinus). Population samples representing the three major morphotypes of Delphinus were obtained from 10 oceanic regions. Our results suggest that short-beaked common dolphins are likely to have originated in the eastern Indo-Pacific Ocean during the Pleistocene and expanded into the Atlantic Ocean through the Indian Ocean. On the other hand, long-beaked common dolphins appear to have evolved more recently and independently in several oceans. Our results also suggest that short-beaked common dolphins had recurrent demographic expansions concomitant with changes in sea surface temperature during the Pleistocene and its associated increases in resource availability, which differed between the North Atlantic and Pacific Ocean basins. By proposing how past environmental changes had an effect on the demography and speciation of a widely distributed marine mammal, we highlight the impacts that climate change may have on the distribution and abundance of marine predators and its ecological consequences for marine ecosystems.

Species tree of a recent radiation: the subfamily Delphininae (Cetacea, Mammalia).

Lineages undergoing rapid radiations provide exceptional opportunities for studying speciation and adaptation, but also represent a challenge for molecular systematics because retention of ancestral polymorphisms and the occurrence of hybridization can obscure relationships among lineages. Dolphins in the subfamily Delphininae are one such case. Non-monophyly, rapid speciation events, and discordance between morphological and molecular characters have made the inference of phylogenetic relationships within this subfamily very difficult. Here we approach this problem by applying multiple methods intended to estimate species trees using a multi-gene dataset for the Delphininae (Sousa, Sotalia, Stenella, Tursiops, Delphinus and Lagenodelphis). Incongruent gene trees obtained indicate that incomplete lineage sorting and possibly hybridization are confounding the inference of species history in this group. Nonetheless, using coalescent-based methods, we have been able to extract an underlying species-tree signal from divergent histories of independent genes. This is the first time a molecular study provides support for such relationships. This study further illustrates how methods of species-tree inference can be very sensitive both to the characteristics of the dataset and the evolutionary processes affecting the evolution of the group under study.

Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus).

Identifying which factors shape the distribution of intraspecific genetic diversity is central in evolutionary and conservation biology. In the marine realm, the absence of obvious barriers to dispersal can make this task more difficult. Nevertheless, recent studies have provided valuable insights into which factors may be shaping genetic structure in the world's oceans. These studies were, however, generally conducted on marine organisms with larval dispersal. Here, using a seascape genetics approach, we show that marine productivity and sea surface temperature are correlated with genetic structure in a highly mobile, widely distributed marine mammal species, the short-beaked common dolphin. Isolation by distance also appears to influence population divergence over larger geographical scales (i.e. across different ocean basins). We suggest that the relationship between environmental variables and population structure may be caused by prey behaviour, which is believed to determine common dolphins' movement patterns and preferred associations with certain oceanographic conditions. Our study highlights the role of oceanography in shaping genetic structure of a highly mobile and widely distributed top marine predator. Thus, seascape genetic studies can potentially track the biological effects of ongoing climate-change at oceanographic interfaces and also inform marine reserve design in relation to the distribution and genetic connectivity of charismatic and ecologically important megafauna.

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.