Evolution of Multicellularity in the Ancestors of Animals: Hydrodynamic Performance and Selective Factors

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ABSTRACT: The origin of multicellular animals from a unicellular protozoan ancestor was a pivotal transition in life’s history.  Choanoflagellate protozoans share a common ancestor with sponges (primitive animals).  We are using choanoflagellates that can be unicellular and can form multicellular colonies of various configurations as model systems to study functional consequences of being multicellular vs. unicellular so that we can gain insights about selective factors that might have affected the evolution of multicellularity.  Before we began our work, it was assumed that forming multicellular colonies permitted the ancestors of animals to escape in size from capture by the unicellular predators that existed before the origin of animals. 

Each choanoflagellate cell propels water by beating a single flagellum and captures bacterial prey on a collar of microvilli around the flagellum.  Choanoflagellates can be free-swimming or attached to surfaces, and colonies can be chains, spheres with the flagella pointing outwards, or cups with the flagella lining the interior (like the flagellated chambers of sponges).  We have used high-speed microvideography and mathematical modeling to study the water flow produced by solitary cells and by colonies of different designs and sizes, and to investigate how such flow affects their ability to swim, catch bacterial prey, and avoid being eaten by different types of protozoan predators similar to those faced by the ancestors of animals:  raptors, suspension feeders, and passive predators.  We have discovered a trade-off between feeding and swimming performance.  We also found that the choanoflagellate forms that produce strong feeding currents are more likely to be sensed and captured by raptorial predators, and that increasing colony size is an effective predator deterrent only against some types of ciliate suspension feeders.  Thus, if the common ancestor of choanoflagellates and animals had the ability shown by choanoflagellates to switch between being unicellular and multicellular, and to alter colony size and configuration in response to variable aquatic environments, that ability to change form (rather than simply becoming multicellular) might have provided a selective advantage to our ancestor.