Collaborative Research: DMS/NIGMS2: Computational and Experimental Analysis of Choanoflagellate Hydrodynamic Performance - Selective Factors in the Evolution of Multicellularity

Trinity University, San Antonio TX

Investigators

Abstract

The evolution of multicellular animals from a unicellular protozoan ancestor was a pivotal transition in the history of life on earth. Choanoflagellates are protozoans that share a common ancestor with animals. They can be unicellular or form multicellular colonies by cell division, so we are studying them to gain insights about the evolution of multicellularity. For multicellularity to have evolved via natural selection in the ancestors of animals, the performance of activities that affected growth, reproduction, and survival would have been better for colonies than for single cells. This project will focus on performance differences between unicellular and multicellular choanoflagellates of activities that affect their fitness: swimming, feeding, and avoiding predation – all of which depend upon the fluid flow around the organisms. This project also will address an important ecological issue. Choanoflagellates and other microscopic protozoans that eat bacteria and are in turn consumed by small animals are a critical link in aquatic food webs. Many protozoans are unicellular, while others form multicellular colonies, but the consequences to swimming, feeding, and escape performance of being single-celled versus multicellular are not yet understood. Choanoflagellates that produce both unicellular and multicellular forms permit us to study the effects of colony formation on the performance of these functions within a single species. A unicellular choanoflagellate has an ovoid cell body and a single flagellum surrounded by a collar of microvilli. The cell swims by waving its flagellum, which also creates a water current that brings bacteria to the collar of prey-capturing microvilli. We will coordinate laboratory experiments with mathematical models and computer simulations that study the hydrodynamic mechanisms that determine the performance of choanoflagellates. Thus, the principles learned from choanoflagellates about the performance of single cells versus multicellular colonies may shed light on mechanisms affecting ecological interactions of aquatic protozoans, as well as on the evolutionary origins of animals. The project will also provide opportunities for undergraduate and graduate students, and postdoctoral scholars to participate in the research. Feeding success and predator avoidance are examples of performance that might have been important selective factors in the evolution from single cells to multicellularity. Our interdisciplinary team will coordinate laboratory experiments, mathematical modeling, and computational simulations to study the hydrodynamics of swimming, feeding, and interacting with predators by unicellular versus colonial choanoflagellates of various configurations, and of pumping and feeding by sponge choanocytes. Models will be developed that probe the effects of cell morphology, number, and arrangement that can be varied in systematic ways not possible with real choanoflagellates. These microscale systems require novel methods that capture cell morphology, geometry of confining structures, dynamic attachment, and detachment of bacteria from choanoflagellate collars, and the chemical and hydrodynamic signals presented to predators. The method of regularized Stokeslets will be advanced to model these complex systems. Lab experiments will use species of choanoflagellates that can be unicellular and form rosette colonies with flagella pointing outwards, or that form cup-shaped colonies that can turn inside-out so the flagella line the cup, as well as protozoan predators on choanoflagellates. Micro videography will be used for particle-tracking velocimetry of flow fields produced by the choanoflagellates, and to measure swimming speeds, feeding rates, and interactions with predators. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.