Drivers of evolutionary changes and community dynamics in ancient Lake Ohrid across taxa: A synthesis of molecular, fossil and sediment record data

• Applicants: Professor Dr. Christian Albrecht; Professor Dr. Thomas Wilke
• Subject Area: Palaeontology ; Evolution, Anthropology
• Term: from 2014 to 2018
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 253046622

• Final Report Year: 2018

Final Report Abstract

The Balkan Lake Ohrid is the most outstanding European ancient lake with an extraordinary species richness and a high degree of endemism in several groups of organisms. However, the processes driving this biodiversity are poorly understood. Preliminary genetic analyses of selected benthic animal groups indicated that most endemic taxa evolved intra-lacustrine over an extended period of time, pointing to an absence of catastrophic events during the geological history of the lake. This hypothesis has, among others, inspired the SCOPSCO ICDP campaign in Lake Ohrid. Starting in early April 2013, the SCOPSCO drilling operation became one of the most successful ICDP lake drilling campaigns ever conducted. Combining molecular clock information derived from extant endemic species with fossil, paleoenvironmental, climatic and geomorphological information, the main goal of our project was to infer the drivers of evolutionary changes and community turnovers in ancient Lake Ohrid across taxa. Specifically, we tested for a) major changes in diversification rates of endemic species groups (SO 1), b) major community and habitat changes (SO 2), and c) the concordance of major geological/limnological/environmental/habitat changes and evolutionary/community changes over time (SO 3). Based on multi-locus phylogenetic and molecular clock analyses of up to eight animal and protist species flocks together with community composition analyses of both recent and fossil species assemblages as well as paleoenvironmental and paleohabitat reconstructions, we were able to answer all questions raised in the original proposal. We found that most endemic taxa studied evolved after the onset of continuous lacustrine conditions in Lake Ohrid c. 1.4 Ma ago. We were even able to demonstrate the existence of a species flock in diatoms, i.e. one of the first confirmed cased in protists. Moreover, lineage-through-time plot and diversification-rate analyses (SP 1) did not reveal deviations from a constant rate of diversification, supporting the hypothesis that the evolutionary trajectories of endemic Ohrid taxa were not “reset” by catastrophic events such as massive lake-level fluctuations and desiccation or salinisation events. The diatom community analyses (SO 2) indicated that environmental filtering is the predominant process structuring communities over the last ca. 1.4 Ma. Moreover, regression model testing indicated that assembly processes depend both on environmental and climate changes. We also used information from community composition (i.e., planktonic to benthic diatom ratios; P:B) to infer past lake-level fluctuations and hence paleo-habitat conditions. Whereas a comparison with geological and bathymetrical information revealed that P:B diatom ratios are relatively well suited for reconstructing lake-level changes during the shallow-water phase of Lake Ohrid (i.e., 1.4–1.0 Ma ago), these ratios do not appear to be reliable proxies for lake-level fluctuations during the deep-water phase (< 1.0 Ma ago). Regarding the concordance of major geological/limnological/environmental/habitat changes and evolutionary/community changes over time (SO 3), we found that paleoenvironment did not directly affect the evolution of traits in diatom groups. However, speciation and extinction rates in endemic species are strongly controlled by a dynamic interplay of geological and environmental factors, as well as species interactions. This project constitutes a novel approach in ancient lake studies. Building upon the synergies offered by the ICDP program, it combined temporarily explicit evolutionary and paleontological information from animal and protist groups with paleoenvironmental data. Moreover, our findings might be of general and theoretical importance in evolutionary biology and macroecology as they provide insights into one of the most debated issues – drivers of speciation. The project led to comprehensive press and TV coverage (incl. FAZ, Spiegel, New Scientist, Fokus Macedonia and 3sat Wissenschaftsmagazin Nano).

Publications

• (2014): Distinct lake level lowstand in Lake Prespa (SE Europe) at the timing of the 74 (75) ka Toba eruption. Climate of the Past, 10, 261-267
  Wagner, B.; Leng, M.; Wilke, T.; Böhm, A.; Panagiotopoulos, K.; Vogel, H.; Lacey, J.; Zanchetta, G. & Sulpizio, R.
  
• (2014): Invaders versus endemics: alien gastropod species in ancient Lake Ohrid. Hydrobiologia, 739, 163-174
  Albrecht, C.; Föller, K.; Hauffe, T.; Clewing, C. & Wilke, T.
  
• (2015): Constant diversification rates of endemic gastropods in ancient Lake Ohrid: Ecosystem resilience likely buffers environmental fluctuations. Biogeosciences, 12, 7209-7222
  Föller, K.; Stelbrink, B.; Hauffe, T.; Albrecht, C. & Wilke, T.
  
• (2016): Assembly processes of gastropod community change with horizontal and vertical zonation in ancient Lake Ohrid: a metacommunity speciation perspective. Biogeosciences, 13, 2901-2911
  Hauffe, T.; Albrecht, C. & Wilke, T.
  
• (2016): Differential resilience of ancient sister lakes Ohrid and Prespa to environmental disturbances during the Late Pleistocene. Biogeosciences, 13, 1149-1161
  Jovanovska, E.; Cvetkoska, A.; Hauffe, T.; Levkov, Z.; Wagner, B.; Sulpizio, R.; Francke, A.; Albrecht, C. & Wilke, T.
  
• (2016): Ecosystem regimes and responses in a coupled ancient lake system from MIS 5b to present: The diatom record of lakes Ohrid and Prespa. Biogeosciences, 13, 3147-3162
  Cvetkoska, A.; Jovanovska, E.; Francke, A.; Tofilovska, S.; Vogel, H.; Levkov, Z.; Donders, T.; Wagner, B. & Wagner-Cremer, F.
  
• (2016): Origin and diversification of Lake Ohrid’s endemic acroloxid limpets: the role of geography and ecology. BMC Evolutionary Biology, 16, 273
  Stelbrink, B.; Shirokaya, A.A.; Föller, K.; Wilke, T. & Albrecht, C.
  
• (2016): Scientific drilling projects in ancient lakes: Integrating geological and biological histories. Global and Planetary Change, 143, 118-151
  Wilke, T.; Wagner, B.; Van Bocxlaer, B. et al.
  
• (2017): The environmental and evolutionary history of Lake Ohrid (FYROM/Albania): interim results from the SCOPSCO deep drilling project. Biogeosciences, 14, 2033-2054
  Wagner, B.; Wilke, T.; Francke, A. et al.