Phytoplankton size: Climatic adaptation and long-term evolution

Coccoliths are micrometer-scale calcite platelets produced by marine single-celled algae (coccolithophores) in the modern oceans and are very abundant as fossils in deep-sea sediments. The size of coccoliths is a useful indirect measure (proxy) for cell s ize, so that we can also reconstruct the cell size of ancient algae based on their fossil coccoliths. Cell size (and coccolith size) is a key parameter of algal physiology and an important indicator of adaptation, on both short and longer time scales. In this project, we study modern, living coccolithophores in combination with the fossil record of their ancestors over the past ca. 60 million years. Rising ocean temperatures will likely cause a more stratified water column, reducing the nutrient (such as nitrate and phosphate) input into upper water layers and increasing the likelihood of nutrient limitation in marine algae. Our experiments with living algae suggest that the effects of phosphate limitation could be intensified under high temperature s tress, as cells require more phosphorus to maintain similar growth and organic carbon production rates. Our results also confirm that not all species respond in the same way to similar nutrient conditions, and that large-celled species appear more sensiti ve to perturbations in nutrient availability than the already well-studied smaller species Emiliania huxleyi. In addition, our culture experiments revealed no significant plasticity in coccolith size (mean and variation) despite extreme experimental growt h conditions. This confirms that the coccolith size variability observed in the fossil record unlikely represents a plasticity response to environmental change of one cosmopolitan species. Rather, an increase (or decrease) in size variation in fossil popu lations points to a changing number of closely related sibling species with different local adaptations and shifts in their abundances due to changing biotic and/or abiotic selection pressures. Marine microfossils constitute the most detailed record of plankton evolution, and time series of their phenotypic (size, shape) variation are perhaps the most direct way of observing evolutionary change. On long, million-year time scales, species-specific responses to climatic change are most likely responsible for the evolutionary patterns we observe in the fossil record. On a macroevolutionary scale, we have demonstrated that coccolithophores were globally more common and widespread, larger, and more heavily calcified before 34 million years ago, in a high-CO 2 greenhouse world. Our study suggests that changes in atmospheric CO2 have, directly or indirectly, exerted an important long-term control on the ecological prominence of coccolithophores as a whole. In contrast, we find no detectable influence of long-t erm climatic change (carbon cycle, temperature) on the size evolution within the fossil lineage of Coccolithus pelagicus, one of the modern species used in culture experiments. Rather, the speciation and extinction of sibling species (fossil morphotypes) , occurring on time scales of 1-4 million years, underpins changes in long-term coccolith size variations observed within this lineage.

Marine phytoplankton form the basis of the marine food chain and are crucial players within the global biogeochemical cycling of carbon and other key elements (e.g. phosphorus, nitrogen). The overall ecological success of marine phytoplankton, but also it s taxonomic diversity and size distribution, determines the efficiency by which fixed carbon is transferred to higher trophic levels and into the deep ocean- and sedimentary carbon reservoirs. Concern is growing that rising temperatures, increased levels of atmospheric CO2 and lowering of ocean pH may disrupt primary productivity in the future oceans. Previous culture experiments on coccolithophores, a prominent group of calcifying marine algae, have shown that the physiological responses to the same env ironmental gradients vary both between and within species. This likely relates to differences in evolutionary history of different lineages and genotypes. However, these observations greatly complicate our predictions of how marine algae may adapt to futu re climatic scenarios. We propose to use a comprehensive approach to study the adaptive response of marine algae to climatic change across ecological and evolutionary time scales. We will combine observations in the fossil record and laboratory experimen ts on living coccolithophores as a basis for innovative evolutionary models that are build as time series of adaptive evolution of algal size around an optimal state. The models will test the influence of environmental variables on this optimum, and deter mine how fast the species are evolving towards their optimal state. By focusing on several key coccolithophore clades, we expect to gain novel insights into species- and genotypic-specific responses in living algae. The outcome of this project will provid e groundbreaking insights into how algae have adapted to past environmental change, and help predict how they may adapt to climatic change in future.