The genomic basis of adaptation in Bottlenose Dolphins (genus Tursiops)

Author: Eleanor Pratt

Pratt, Eleanor, 2020 The genomic basis of adaptation in Bottlenose Dolphins (genus Tursiops), Flinders University, College of Science and Engineering

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The application of ecological genomic techniques to marine biodiversity is becoming increasingly recognised, with a growing number of studies utilising genomics to address population diversification, structure and connectivity in a range of marine species. This has primarily focused on species of importance to recreational and commercial fishing, but is now being expanded to include megafauna, such as marine mammals. While genomic studies of cetacean (whale and dolphin) evolution are relatively prevalent, much of this research concerns the macroevolutionary transition of this lineage from land to the aquatic environment. Microevolutionary genomic differentiation among and within closely related species on the other hand, has only recently begun to be investigated. Bottlenose dolphins (genus Tursiops) exhibit repeated inshore and offshore ecotypes around the world, with fine-scale population genetic structure typically found within the inshore lineages. The drivers of ecotype formation and population differentiation have until now not been investigated using genomic techniques and formal testing of genotype-environment associations. This line of study provides an excellent opportunity to better understand the environmental drivers of speciation and differentiation in marine species. This is becoming increasingly important with ongoing anthropogenically-induced climate change rapidly impacting on marine species and altering their ecosystems worldwide.

This study uses genomic datasets to clarify the evolution of bottlenose dolphins at species and population levels. The relationship between divergence and ecological heterogeneity is explored and empirically tested, revealing the genomic basis of potential adaptations to selective pressures and environmental heterogeneity. Briefly, four separate bottlenose dolphin species or subspecies were supported for the Southern Hemisphere, each with unique evolutionary histories shaped by interactions with their respective habitats. This includes the common bottlenose dolphin (T. t. truncatus) widely distributed throughout offshore waters of the Southern Hemisphere, and its recognised subspecies in inshore waters of the southwest Atlantic Ocean (T. t. gephyreus). Evidence was also found for genomic divergence between the Indo-Pacific bottlenose dolphin (T. aduncus) in eastern Australia and the proposed species (T. australis) in coastal southern Australia, suggested here to represent a subspecies of T. aduncus (southern Australian bottlenose dolphin, SABD). Genomic differentiation between the inshore and offshore ecotypes revealed adaptations that are potentially most important to early stages of inshore colonisation and provided evidence for parallel evolution in the inshore ecotype. Repeated selection on over one hundred candidate genes across the inshore lineages based on a genomic dataset of over 18,000 loci, revealed potential adaptations of several major bodily systems including the cardiovascular, sensory, musculoskeletal, gastrointestinal, energy production, nervous and osmoregulatory systems. This was hypothesised as a response to divergent selection pressures associated with environmental and ecological disparity, such as differences in depth and prey abundance and distribution between the inshore and offshore habitats.

At a population level, fine-scale neutral population genomic structure was found in bottlenose dolphins along the eastern and southern Australian coasts (T. aduncus and SABD, respectively). In both cases, this is likely associated with isolation by distance, strong social structure and natal philopatry. On the other hand, environmental gradients over small geographical distances were empirically shown to shape patterns of adaptive differentiation in these populations. Sea surface temperature and salinity gradients were highly correlated with SABD adaptive differentiation, while heterogeneity in productivity and habitat and oceanographic features were suggested to be most influential on T. aduncus. Several genes were found as candidates for driving adaptation of bottlenose dolphins to these particular environmental variables. This includes potential modification of the kidneys and ion transport pathways in response to hypersalinity in South Australia's Spencer Gulf and changes in digestion and metabolism systems to adapt to significant changes in productivity in areas of the New South Wales coast. Substantial overlap in the bodily systems and specific genes under selection was found among datasets of the three data chapters, suggesting key pathways involved in parallel adaptation of different lineages of inshore bottlenose dolphins. Selection on many of these same pathways and genes have also been discovered in previous studies across several marine taxa, suggesting that they are not only important to environmental adaptation in bottlenose dolphins, but also to other marine species.

This study provides crucial information about drivers of species and population divergence and adaptive evolution in cetaceans. With climate change already causing major restructuring of ecological conditions and species distributions in the world’s oceans, having a better understanding of the adaptive capacity of local populations will become increasingly important. Findings of this thesis can therefore, be incorporated into management plans to ensure well-informed and effective conservation strategies to support marine ecosystems into the future.

Keywords: ddRADseq, genomics, bottlenose dolphins, cetaceans, Tursiops, seascape genomics, parallel evolution, comparative genomics, phylogenomics, population structure, Australia, genotype-environment association, redundancy analysis

Subject: Environmental Science thesis

Thesis type: Doctor of Philosophy
Completed: 2020
School: College of Science and Engineering
Supervisor: Luciana Moller