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  1. Evaluation Summary:

    In this study, the authors develop a model to understand the simplest form of collective migration represented by a pair of cardiopharyngeal progenitor cells. They propose that the collective migrates as a "supracell", with leader cells assuming a greater protrusive capability and trailer cells assuming greater retractive capability. They meticulously study the effects of leader-trailer and cell-matrix adhesivity, intracellular force distributions and noise on robustness of cell migration. They corroborate their simulation results with experiments. Overall, this study comprehensively demonstrates that migrating as a collective leads to more mechanically efficient and persistent migration than as a single motile cell.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)

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  2. Reviewer #1 (Public Review):

    In this manuscript, authors develop a computational model of migrating pairs of cardiopharyngeal progenitors in Ciona model to describe their properties during migration. Most of the predictions drawn from the simulations are corroborated experimentally in vivo. The polarized migrating pair of progenitors represent a minimum unit of collective migration showing essentially that "two cells are better than one".

    The simulation of the migrating cell pair is based on Cellular Potts Model and uses cell morphology as a proxy to model different mechanical and cellular forces that generate specific cell shapes during migration. The model seems to faithfully reproduce the in vivo observations. The arguments describing the model are well explained. The model thus provides a number of predictions pertaining the migrating cell collectives that can be tested in vivo using genetic and molecular tools. The authors then test some of the predictions prompting them to conclude that the migrating progenitor pair present the simplest model of collective migration, in which the two cells are intercellularly coupled and their polarization occurs across the two-cell continuum, thus forming a supracellular collective. This cell collective displays hierarchy, which favors linear arrangement conferring directionality and persistence in migratory behavior. While some conclusions are well justified and the experimental evidence corroborates the simulations, at few points the conclusions are more speculative; the figure panels not always match the manuscript text. The concept that the migrating pair can deform the overlaying endoderm is the least developed and not probed in vivo. In summary, the computational model represents a powerful tool to examine directional migration of polarized cell collectives with similar characteristics allowing for studying how biomechanical cues integrate with molecular signals across group of cell collectives to coordinate their behavior.

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  3. Reviewer #2 (Public Review):

    In this study, the authors develop a model to understand the collective migration of migrating pairs of cardiopharyngeal progenitor cells. This represents an simplest form of collective migration with two cells. They propose that the collective migrates as a "supracell", with leader cells assuming a greater protrusive capability and trailer cells assuming greater retractive capability. They meticulously study the effects of leader-trailer and cell-matrix adhesivity, intracellular force distributions and noise on robustness of cell migration. They corroborate their simulation results with experiments. Overall, this study comprehensively demonstrates that migrating as a collective leads to more mechanically efficient and persistent migration than as a single motile cell. A particular strength of the paper is that the authors have done an excellent job of explaining how the Cellular Potts Model works and how they chose to represent specific biological details using this modelling environment. The model is also likely to provide a useful framework for development of models of more complex examples of collective migration.

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