Ecology and Evolution of Fishes of the Southern Ocean – A multidimensional molecular approach

The Antarctic and the surrounding Southern Ocean contain delicate and unique ecosystems, characterised by a cold climate, a seasonal photoperiod, remote location and a endemic fauna. Compared to other oceans, the Southern Ocean exhibits low species richness, but despite this, the Southern Ocean is still characterized as an evolutionary hotspot. The adaptive radiation of the notothenioids, the predominant clade of fishes in the Southern Ocean have evolved from a common benthic ancestor without a swim bladder. During their repeated diversification into the pelagic environment they have developed unique adaptations such as anti-freeze glycoproteins (AFGP), reduced ossification or even the loss of haemoglobin. Due to their rapid diversification, and their ecological and morphological diversity, these fishes pose a unique study system to address questions at the interface between ecology and evolution. Here we used DNA metabarcoding to assess the prey and microbiome composition as well as restriction site associated DNA sequencing to assess the genomic divergence of these fishes. Due to the value and the limited availability of samples from the Southern Ocean, optimisation of methods was conducted with less valuable samples. Therefore, DNA metabarcoding techniques were optimised using North Sea plaice (Pleuronectes platessa) from various locations of the North Sea and the Eastern English Channel. A 313 bp fragment of the cytochrome c oxidase subunit I (COI) was amplified and sequenced for prey item identification in the stomach and a 450 bp region of the 16S rRNA gene to investigate microbiome composition in the gut system. We detected great homogeneity and only subtle differences in the prey and microbiome composition; we were largely able to confirm previously known prey items identified through visual assessment of the stomach. Baseline data is often hard to obtain, especially for remote places and processes that may span a century, or longer. Here, we compared the microbiome composition of members of the genus Trematomus in a historic and contemporary context, using samples stored in natural history museums (NHMs) and from current research expeditions. Unfortunately, NHM samples are often preserved in formaldehyde (formalin), which affects DNA and complicates genetic studies due to chemical reactions. Processing of NHM samples was characterised by large dropout rates, but despite this, we were able to obtain reliable microbiome composition data (16S rRNA) from 26 historic samples. These data showed a correlation in change of microbiome composition with fish size as well as year of catch, pointing to a microbiome shift throughout ontogeny and between samples from different decades. A comparison with contemporary samples indicated that the intestinal microbiome of Trematomus may have drastically changed within the last century. Despite tremendous efforts that went into understanding the prey and microbiome composition of fishes in the SO, detailed knowledge is still scarce. Here, we assessed the prey and microbiome composition of a wide range of notothenioid fishes. We detected 79 previously unknow prey item classes, which were mostly soft-tissued taxa or larger animals, that were not ingested whole. The prey and microbiome composition were highly correlated, indicating a strong link between the diet and the associated microbiome. Lastly, diet and microbiome compositions were best predicted by phylogenetic distance for benthic notothenioids, indicating stronger niche segregations, while non-benthic species are possibly still diverging or have secondarily overlapped. Lastly, we assessed the genomic divergence of two species of the genus Trematomus using restriction site associated DNA sequencing. Trematomus eulepidotus and T. loennbergii have recently diverged and exhibit similar life history, however, inhabit differing habitats. Interspecific analysis between T. eulepidotus and T. loennbergii revealed diffuse species boundaries. Hybridisation, historic or contemporary introgression, incomplete lineage sorting or even incomplete speciation may all be key factors contributing to blurring the taxonomic boundaries. Intraspecific analysis revealed clear formation of subpopulation. While driving factors for creating such subpopulations remain unclear for T. loennbergii , for T. eulepidotus habitat differences appear to be the main driver. Here we present important information on the evolution In this PhD thesis we present important insights into the ecology and the evolution of fishes of the Southern Ocean with a special interest in the genus Trematomus. In addition to providing novel knowledge on the trophic food web in the Southern Ocean as well as the gastrointestinal microbiome of SO fishes, both in a historical as well as contemporary context, we highlight the potential of metabarcoding studies to address in parallel evolutionary and conservation biology questions. We present novel evolutionary insights regarding the diversification of two members of the genus Trematomus. Findings from this thesis have important implications, when considering the ecology of the teleost fauna, especially with respect to past and future climate change scenarios.

Publication year:2019

Accessibility:Open