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.

Movements and behaviour of blue whales satellite tagged in an Australian upwelling system.

Knowledge about the movement ecology of endangered species is needed to identify biologically important areas and the spatio-temporal scale of potential human impacts on species. Blue whales (Balaenoptera musculus) are endangered due to twentieth century whaling and currently threatened by human activities. In Australia, they feed in the Great Southern Australian Coastal Upwelling System (GSACUS) during the austral summer. We investigate their movements, occupancy, behaviour, and environmental drivers to inform conservation management. Thirteen whales were satellite tagged, biopsy sampled and photo-identified in 2015. All were genetically confirmed to be of the pygmy subspecies (B. m. brevicauda). In the GSACUS, whales spent most of their time over the continental shelf and likely foraging in association with several seascape variables (sea surface temperature variability, depth, wind speed, sea surface height anomaly, and chlorophyll a). When whales left the region, they migrated west and then north along the Australian coast until they reached West Timor and Indonesia, where their movements indicated breeding or foraging behaviour. These results highlight the importance of the GSACUS as a foraging ground for pygmy blue whales inhabiting the eastern Indian Ocean and indicate the whales' migratory route to proposed breeding grounds off Indonesia. Information about the spatio-temporal scale of potential human impacts can now be used to protect this little-known subspecies of blue whale.

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.

Atypical residency of short-beaked common dolphins (Delphinus delphis) to a shallow, urbanized embayment in south-eastern Australia.

Short-beaked common dolphins (Delphinus delphis) are typically considered highly mobile, offshore delphinids. This study assessed the residency of a small community of short-beaked common dolphins in the shallow, urbanized Port Phillip Bay, south-eastern Australia. The ability to identify common dolphins by their dorsal fin markings and coloration using photo-identification was also investigated. Systematic and non-systematic boat surveys were undertaken between 2007 and 2014. Results showed that 13 adult common dolphins and their offspring inhabit Port Phillip Bay, of which 10 adults exhibit residency to the bay. The majority of these adults are reproductively active females, suggesting that female philopatry may occur in the community. Systematic surveys conducted between 2012 and 2014 revealed that the dolphins were found in a median water depth of 16 m and median distance of 2.2 km from the coast. The shallow, urbanized habitat of this resident common dolphin community is atypical for this species. As a result, these common dolphins face threats usually associated with inshore bottlenose dolphin communities. We suggest that the Port Phillip Bay common dolphin community is considered and managed separate to those outside the embayment and offshore to ensure the community's long-term viability and residency in the bay.

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.

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.

The use of carcasses for the analysis of cetacean population genetic structure: a comparative study in two dolphin species.

Advances in molecular techniques have enabled the study of genetic diversity and population structure in many different contexts. Studies that assess the genetic structure of cetacean populations often use biopsy samples from free-ranging individuals and tissue samples from stranded animals or individuals that became entangled in fishery or aquaculture equipment. This leads to the question of how representative the location of a stranded or entangled animal is with respect to its natural range, and whether similar results would be obtained when comparing carcass samples with samples from free-ranging individuals in studies of population structure. Here we use tissue samples from carcasses of dolphins that stranded or died as a result of bycatch in South Australia to investigate spatial population structure in two species: coastal bottlenose (Tursiops sp.) and short-beaked common dolphins (Delphinus delphis). We compare these results with those previously obtained from biopsy sampled free-ranging dolphins in the same area to test whether carcass samples yield similar patterns of genetic variability and population structure. Data from dolphin carcasses were gathered using seven microsatellite markers and a fragment of the mitochondrial DNA control region. Analyses based on carcass samples alone failed to detect genetic structure in Tursiops sp., a species previously shown to exhibit restricted dispersal and moderate genetic differentiation across a small spatial scale in this region. However, genetic structure was correctly inferred in D. delphis, a species previously shown to have reduced genetic structure over a similar geographic area. We propose that in the absence of corroborating data, and when population structure is assessed over relatively small spatial scales, the sole use of carcasses may lead to an underestimate of genetic differentiation. This can lead to a failure in identifying management units for conservation. Therefore, this risk should be carefully assessed when planning population genetic studies of cetaceans.

Thermal windows on the trunk of hauled-out seals: hot spots for thermoregulatory evaporation?

Seals have adapted to the high heat transfer coefficient in the aquatic environment by effective thermal insulation of the body core. While swimming and diving, excess metabolic heat is supposed to be dissipated mainly over the sparsely insulated body appendages, whereas the location of main heat sinks in hauled-out seals remains unclear. Here, we demonstrate thermal windows on the trunk of harbour seals, harp seals and a grey seal examined under various ambient temperatures using infrared thermography. Thermograms were analysed for location, size and development of thermal windows. Thermal windows were observed in all experimental sessions, shared some common characteristics in all seals and tended to reappear in similar body sites of individual seals. Nevertheless, the observed variations in order and location of appearance, number, size and shape of thermal windows would imply no special anatomical site for this avenue of heat loss. Based on our findings, we suggest that, in hauled-out seals, heat may be transported by blood flow to a small area of the wet body surface where the elevation of temperature facilitates evaporation of water trapped within the seals' pelages due to increased saturation vapour pressure. The comparatively large latent heat necessary for evaporation creates a temporary hot spot for heat dissipation.