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Local adaptation in the presence of gene flow in Patagonian and Antarctic Nacella limpets

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Pöhlmann, K. (2011): Local adaptation in the presence of gene flow in Patagonian and Antarctic Nacella limpets , PhD thesis, University of Bremen.
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Abstract:

The classical belief that speciation needs geographical isolation has raised the question how the huge amount of biodiversity can be explained in an open environment like the ocean that is characterized by the absence of strict barriers to gene flow over large geographical scales. Many theoretical approaches have contested that classical belief showing how speciation can take place in the background of gene flow rendering natural selection as a potent evolutionary force. However, most of the empirical population genetic studies aiming at speciation processes apply neutral molecular markers which do not respond to selective forces and therefore do not allow for statements on the actual roles of selection causing ecologically based barriers to gene flow. The present study‘s superordinate aim was to reconstruct the evolutionary history of South American and Antarctic patellogastropods of the genus Nacella. The central aspects of the thesis were the investigation of the actual roles of gene flow barriers and natural selection in processes causing speciation and population divergence. In order to fulfill this task a wide range of markers, both neutrally evolving and under selection, was applied to reveal gene flow patterns and local adaptation. The ACC is one of the most prominent physical barriers in the ocean. Its origin around 35 Ma before present should therefore be reflected in the timing of the divergence of Nacella. Molecular dating approaches carried out in this thesis with three different nuclear and mitochondrial genes (COI, 16S, 18S) revealed the timing of speciation of Nacella to be much younger than the proposed onset of the ACC (~ 10 Ma). Gene flow must, therefore, have been possible after the ACC had already been fully established until the Miocene 10 Ma ago. This time coincides with the second major cooling of Antarctica that led to the glaciation of the Antarctic Peninsula and most likely increased the selection for physiological and genetic adaptation on both sides of the Drake Passage. The present example highlights that the mere occurrence of the ACC alone was not sufficient to promote speciation between Antarctic and South American species. It most likely needed the additional influence of natural selection summoned by climatic changes. 135 Summary . A more detailed view on the impact of natural selection was obtained by population genetic studies of the two South American species N. magellanica and N. deaurata. They largely occur in sympatry but exhibit differences in vertical zonation along the tidal gradient. N. magellanica mainly inhabits the shallow intertidal areas and is exposed to tidal emersion twice a day. N. deaurata occurs in the deeper subtidal that is normally not heavily affected by the tidal cycles. Neutral markers (COI and seven microsatellites) reveal Southern South America to be a high gene flow environment without any genetic divergence between both morphotypes rendering them as morphotypes caused by phenotypic plasticity. The addition of genetic markers under selection (Hsp70) revealed a deep divergence between the two morphotypes. These contradicting results show that divergent selection in sympatry can cause ecologically important genomic regions to resist gene exchange, whereas in other parts of the genome gene flow continues. The genetic divergence in Hsp70 has most likely established in phases of geographical isolation of populations on Atlantic and Pacific sides of South America summoned by glacial maxima. Upon secondary contact after the Last Glacial Maximum had ended, gene flow between those populations was not restricted as seen in neutral markers. The divergence in Hsp70, however, displays how divergent selection maintains adaptive divergence in parts of the genomes in order to ensure adaptability to the environmental constraints along a tidal gradient. Physiological experiments in which individuals of N. magellanica and N. deaurata were exposed to air furthermore revealed some of the potent drivers of ecological selection that maintain genetically disrupted gene pools. The differences in vertical zonation are reflected in lower adaptability to desiccation stress and elevated temperatures summoned by tidal emersion as seen in higher heat-shock response (HSR) and enzymatic antioxidant defense levels in subtidal N. deaurata. The present study highlights the complex interplay of geographical isolation and natural selection in the evolutionary history of Nacella. The addition of genetic markers under selection provides a powerful tool to understand the importance of natural selection and local adaption as common evolutionary forces that are largely undetected by neutral marker approaches.

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