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

多细胞动物从单细胞原生动物的祖先进化而来，是地球生命史上的一个关键转变。脊椎动物是与动物有共同祖先的原生动物。它们可以是单细胞的，也可以通过细胞分裂形成多细胞克隆，所以我们正在研究它们，以获得对多细胞进化的见解。如果多细胞是通过动物祖先的自然选择进化而来的，那么影响生长、繁殖和生存的活动对群体的表现会比对单个细胞更好。这个项目将集中在单细胞和多细胞脊椎动物之间的性能差异，这些活动影响它们的健康：游泳、进食和避免捕食--所有这些都取决于有机体周围的流体流动。该项目还将解决一个重要的生态问题。鞭毛虫和其他以细菌为食并被小动物消耗的微小原生动物是水生食物网中的关键一环。许多原生动物是单细胞的，而其他原生动物则形成多细胞群体，但单细胞与多细胞相比对游泳、取食和逃逸性能的影响尚不清楚。脊椎动物同时产生单细胞和多细胞形式，使我们能够研究菌落形成对单个物种内这些功能表现的影响。单细胞尾鞭毛虫具有卵圆形细胞体和被微绒毛领包围的单个鞭毛。细胞通过挥动鞭毛来游泳，这也创造了一股水流，将细菌带到捕捉猎物的微绒毛的领子上。我们将把实验室实验与数学模型和计算机模拟相结合，研究决定脊椎动物性能的流体力学机制。因此，从脊椎动物身上学到的关于单细胞与多细胞群体性能的原理可能有助于阐明影响水生原生动物生态相互作用的机制，以及动物的进化起源。该项目还将为本科生和研究生以及博士后学者提供参与研究的机会。取食成功和避免捕食者是表现的例子，这些表现可能是从单细胞进化到多细胞的重要选择因素。我们的跨学科团队将协调实验室实验、数学建模和计算模拟，以研究各种配置的单细胞和集群脊椎动物与捕食者游泳、取食和相互作用的水力学，以及海绵脊椎动物抽吸和取食的水力学。将开发模型来探索细胞形态、数量和排列的影响，这些影响可以以系统的方式改变，而真正的脊椎动物是不可能的。这些微型系统需要新的方法来捕捉细胞形态、限制结构的几何形状、细菌的动态附着和从脊椎动物的项圈上脱落，以及提供给捕食者的化学和水动力学信号。提出了用正则化斯托克斯莱斯方法对这些复杂系统进行建模。实验室实验将使用单细胞的脊椎动物物种，形成鞭毛朝向外的玫瑰丛生群体，或者形成杯状群体，使鞭毛排列在杯子上，以及脊椎动物上的原生动物捕食者。显微摄像技术将被用来对脊椎动物产生的流场进行粒子跟踪测速，并测量游泳速度、进食率以及与捕食者的相互作用。这一奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

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.