Divergence and Adaptive Capacity of Marine Keystone Species

Katharina Fietz

Abstract

A multitude of anthropogenic actions ranging from overexploitation, pollution, and eutrophication to the introduction of invasive species impact the marine environment today (Jansson & Dahlberg 1999; Islam & Tanaka 2004; Pauly et al. 2005; Molnar et al. 2008). In combination with rapid environmental alterations brought about by climate change, these factors confer increasing pressure on marine organisms. An understanding of population divergence patterns, population sizes, and local adaptive capacities is an important baseline for the design of sustainable resource management measures and effective conservation actions. In this thesis, I took a population genetic approach to shed light on the above features of three different keystone organisms in the North Atlantic and Baltic Sea ecosystems. In Chapter 2, my colleagues and I combined modern and historic nuclear and mitochondrial genetic markers with zooarchaeological, demographic, and life history data, in order to investigate the processes that drove colonization, extinction, and re-colonization of two grey seal subspecies (Halichoerus grypus grypus and Halichoerus grypus atlantica) in the Baltic Sea and North Sea. We revealed that the two subspecies diverged ca. 4,200 yrs BP due to an isolation process that was presumably initiated by cooling and increasing ice cover of the Baltic Sea 3,500-4,500 yrs BP, and upheld by continued anthropogenic disturbance. We further discovered that the historic grey seal population in (the geographically intermediate) Danish waters was genetically connected to the Central Baltic Sea, while recolonizers of the same region today stem from either North Sea or Baltic Sea. Lastly, we identified one location in the southwest Baltic Sea that harbors admixed individuals, suggesting that this might be a place of subspeciesreconnection in the near future. Chapter 3 focuses on the extent of gene flow between the only two known North Atlantic humpback whale (Megaptera novaeangliae) breeding grounds, and its effect on the effective size of the breeding population in Cape Verde. Humpback whales in the North Atlantic have undergone a drastic depletion during the 19th and 20th century due to heavy whaling activity (Smith & Reeves 2003). Only within the last 60 years have they had a chance to recover thanks to dedicated conservation efforts (Best 1993). Our study was able to show that humpback whales in Cape Verde have likely undergone several historic and more recent population declines, and today may be at or below a minimum viable population size. In addition, we showed that the amount of long-term average gene flow between Cape Verde and the only other known breeding ground in the West Indies is very limited, and indeed is of the same level of magnitude as genetic differentiation in humpback whales between ocean basins (Jackson et al. 2014). In Chapter 4, my colleagues and I investigated genome-wide population divergence patterns in two economically and ecologically important sand lance species (Ammodytes tobianus and Hyperoplus lanceolatus) in the Baltic Sea and North Sea. This study further took one step beyond focusing on the genome alone, and additionally drew on information about the associated fish gut and environmental water bacterial communities. Three findings emerged: Firstly, the Baltic Sea harbors unique genetic populations of sand lances that are differentiated from the North Sea. Genomic regions showed elevated divergence not only as a potential response to salinity- and SST-related natural selection, but these regions also correlated with the relative bacterial composition of the water. This could hint at a potential influence of environmental microbes on the adaptive genetic divergence of these marine fishes. Secondly, we confirmed that Baltic Sea A. tobianus exist as two genetic stocks co-occurring in the same habitat. Thirdly, the gut microbial communities of sand lances are not a mere reflection of environmental microbes, but rather the fishes themselves seem to excerpt some degree of internal control and selection. The application of a range of molecular tools and their integration with environmental, count, life history, and microbial data in the thesis presented here hopefully demonstrate the usefulness of applying genetic methodology to the investigation of marine populations. I believe that this work further illustrates the wide utility of genetic and genomic methodology in a conservationmanagement framework. In the case of the Northern European grey seal, the findings of our study highlight the importance of distinguishing grey seals as different genetic and demographic units in Skagerrak, Kattegat, and the southwest Baltic when setting annual decimation quota (Chapter 2). Regarding the small North Atlantic humpback whale breeding population in Cape Verde, our work suggests that this population requires particular management attention, as it may be vulnerable to stochastic effects of inbreeding and to anthropogenic disturbances (Chapter 3). Lastly, our sand lance study results suggest that the different sand lance species differ in their population divergence patterns, and that as a result connectivity of different areas might not be comparable across species (Chapter 4). As such, it might be advisable to reconsider the current management scheme that is treating all occurring sand lance species as one.

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