Optimality and trait based approaches to sympatric speciation and sympatric co-evolution of predator and prey traits in marine plankton

Marine microorganisms are responsible for roughly half of the Earth’s primary production, circa half of the carbon dioxide sink and oxygen production on Earth. Marine plankton organisms are an important part of global biogeochemical models, which simulate the effects of current global change, e.g., increased CO2 levels, increased temperature, or increased eutrophication on ecosystem functioning and community dynamics. However, such models rarely account for the adaptation of marine microorganisms, which are able to evolve rapidly. While some global models deal with the extinction of species and loss of biodiversity, they do not account for speciation. Due to a highly unstructured marine environment with no clear boundaries, understanding sympatric speciation, which is the speciation without geographic isolation, in plankton is particularly important. However, sympatric speciation in terrestrial systems has gained much more attention while in marine systems it was largely ignored. The most famous example of sympatric speciation are Darwin’s finches, which diversified by specialisation on different resources. But despite the large number of existing speciation models, a concrete mechanism which allows for sympatric speciation via specialisation, as suggested by Darwin, has been difficult to pin down. Therefore, in the first part of the thesis we propose a concrete mechanism of sympatric speciation via specialisation and resource partitioning allowing predators to reduce competition and create new ecological niches. The key to this mechanism are the reduced costs in the specialisation trade-off, whereby the improved ability to eat the preferred prey (gain) over-compensates the reduced ability to eat the less-preferred prey (cost). Such "plus-zero sum game” increases the grazing pressure on prey, which in turn may respond by changing traits, e.g., the specific growth rate, in order to escape the grazing pressure. Building on this mechanism, in the second part of the thesis we explore sympatric speciation in the face of simultaneous co-evolution of a prey trait (growth rate) and a predator trait (specialisation) in a simple predator-prey interaction model. We find that the space defined by all combinations of predator and prey traits can be divided into three regions: (1) the speciation space, where the combinations of traits allow speciation leading to the establishment of two sympatric predator species; (2) the vanishing speciation space, i.e. the range of combinations allowing only ephemeral speciation and (3) the displacement space, where the resident predator is displaced by a single mutant. We also introduce and discuss some further novel concepts, e.g., evolutionary time landscape, speciation threshold and prey-equality space. We conclude that prey species can adjust traits as a response to increased predation. This raises the question of how both trophic levels would adapt to changing environmental conditions. While some studies investigated the evolutionary response of marine plankton to increased temperature, CO2 and acidification, changes in the marine biodiversity as a consequence of increased nutrient concentration (i.e. eutrophication) has not been intensively studied yet. Moreover, the density-independent mortality (DIM) in the ocean was largely ignored and not treated separately from the grazing mortality. Hence, in the third part of the thesis we examine the occurrence of sympatric speciation and the dynamics of a marine plankton community as a function of three changing quantities: environmental nutrient load, DIM of phytoplankton, and adaptive specialisation of zooplankton. Particularly we study the coevolution of plankton and the resource use efficiency in a four-species predator-prey interaction model at different environmental nutrient concentrations and density-independent mortalities of the prey. The results imply that increasing nutrient concentration in our model: (1) promotes biodiversity, (2) decreases the effect of DIM of phytoplankton on biodiversity, (3) changes domination from prey species to predators, and (4) decreases overall system productivity. This thesis emphasises the importance of traits and trade-offs for understanding the adaptive behavior of marine plankton. Fast evolutionary changes and density-independent crashes of populations in marine plankton necessitate the consideration and better representation of evolutionary processes in global biogeochemical models in order to better project the impacts of climate change on marine ecosystems. Sympatric speciation deserves particular attention due to the absence of clear geographic barriers in the marine environment.


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