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

Abstract

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.

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

“…This result is consistent with a previous microsatellite study that suggested differentiation between dolphins of these two sites [31], although this separation was not disclosed by neutral SNP study [29]. A recent GEA study in a closely related species, the Indo-Pacific bottlenose dolphin (T. aduncus), did not disclose similar separation between localities in the southern coast of Western Australia [20]. This is potentially due to difference in habitat use between the two species, with bottlenose being generally found closer to shore as compared to common dolphins that have a more offshore distribution.…”

“…Each local habitat, or bioregion, exhibits different environmental gradients, such as temperature, current velocity, and salinity, which could be impacting common dolphins and their prey distribution in southern Australia. Differentiation between locally adapted populations despite metapopulation gene flow, has been previously described for other marine taxa along southern Australia (e.g., Haliotis [36,37], and Nerita [87]), and in another delphinid (e.g., T. aduncus [20]). Effects of climate change may differ between adapted populations, with local populations exhibiting low adaptive diversity, such as those in coastal protected environments or embayments, perhaps more vulnerable to such effects (e.g., [20,40,88]).…”

“…Differentiation between locally adapted populations despite metapopulation gene flow, has been previously described for other marine taxa along southern Australia (e.g., Haliotis [36,37], and Nerita [87]), and in another delphinid (e.g., T. aduncus [20]). Effects of climate change may differ between adapted populations, with local populations exhibiting low adaptive diversity, such as those in coastal protected environments or embayments, perhaps more vulnerable to such effects (e.g., [20,40,88]). Thus, neutral and adaptive variation are both relevant to conservation for maintaining high standing genetic variation and evolutionary potential across the southern Australia's common dolphin metapopulation.…”

“…In toothed whales (Odontoceti), most studies of adaptations using genomic markers have focused on a macroevolutionary perspective, while studies investigating ecological specialisation on a microevolutionary level have been documented only for a few species. This includes ecotype adaptations of killer whales (Orcinus orca [16]), spinner dolphins (Stenella longirostris [17]), finless porpoises (Neophocaena phocaenoides [18,19]), and bottlenose dolphins (Tursiops aduncus [20], and T. truncatus [21]). Despite these examples, population-level studies of microevolutionary processes remain highly under documented in Odontocetes, specifically in small cetaceans.…”

Molecular Assessments, Statistical Effectiveness Parameters and Genetic Structure of Captive Populations of Tursiops truncatus Using 15 STRs

“…Regarding the remarkable diversity found, we did not rule out that it could be related to other species such as Tursiops aduncus ( T. aducus ) that could have been confused with Tursiops truncatus truncatus ( Tursiops t. truncatus ). The genetic characterization using STRs and mtDNA has shown the presence of T. aducus in coastal waters of southern Australia [ 61 ]. Unfortunately, the absence of non-nuclear genetic markers (i.e., control, D-loop, and Cytochrome regions) to clarify this doubt limited our study [ 22 , 49 , 62 ].…”