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  1. Evaluation Summary:

    This is a strong and concise paper using mathematical modelling to explore the conditions under which reproductive division of labour can evolve. It clarifies open questions regarding scenarios where specialising individuals experience diminishing returns from engaging in division of labour. The authors provide a comprehensive set of analyses highlighting when division of labour can evolve under such conditions and when not. The paper's primary claims are supported by the analysis provided, and the paper is likely of interest to evolutionary biologists, ecologists, computational biologists, and microbiologists.

    (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):

    The paper consists of two parts.

    The first part deals with "the three pathways to division of labour". It builds on a mathematical model showing that division of labour can evolve when (1) there are accelerating returns for individuals from specialisation, (2) there are pre-existing differences between individuals such that some individuals are predisposed for one task or the other, and (3) there is reciprocal specialisation leading to synergistic efficiency benefits at the group level. This model recovers the findings by Rueffler et al. 2012. This part is very well written and reads more like a review, bringing specialised and non-specialised readers onto the same page.

    The second part focusses on pathways (2) and (3), where individual returns can be diminishing, and thus the evolution of division of labour is more difficult to explain. This part is motivated by a recent paper by Yanni et al. 2020 in eLife showing that topological constraints (e.g. small network of individuals, limited number of neighbours) are essential to favour division of labour with diminishing returns. The authors challenge this view and provide an in-depth analysis on topological constraints. They show that such constraints in combination with pre-existing differences between individuals and reciprocal specialisation are indeed conducive for the evolution of division of labour, but not essential. They show that when the benefit of cooperation is larger for neighbours than for the cooperator than division of labour can evolve with diminishing returns even in the absence of topological constraints. This is a key new insight. But perhaps even more important, the authors highlight that pathways (2) and (3) rely on the assumption that individuals have access to information from neighbours to coordinate their actions at the group level. The authors show that division of labour cannot evolve with diminishing returns when such information is absent. And because mechanisms of information collection and coordination are likely to only evolve once division of labour is already in place, the authors argue that topological constraints might play a minor role in driving the initial evolutionary steps towards division of labour.

    In brief, this is a very insightful paper and significantly advances our theoretical and conceptual understanding of division of labour. It will spur future theoretical and empirical work in the field, and for the latter, the authors present guidelines of how to test the theory.

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  3. Reviewer #2 (Public Review):

    This is a very interesting paper on the evolution of division of labor. In particular, the authors explore the impact of topology, the convexity and concavity of fitness returns on investment, and different biological 'modalities' through which division of labor may arise. This is a difficult topic to study as, in most lineages, division of labor evolved long ago, and thus cannot be directly studied in the lab. Further, many theoretical predictions have proven difficult to directly test. This manuscript furthers our understanding of the underlying theory of the evolution of division of labor, and presents a means to test which modality is responsible for the emergence of division of labor in different cases.

    However, there are a few caveats worth mentioning. Comparisons to previous works are not always clear. Different models built with different assumptions can produce different predictions; however, that does not mean they disagree, only that they describe different scenarios. Further, the model used here allows an entity to give away all of its 'viability,' making it unclear how it continues to live and function. Finally, the order in which division of labor and 'patterning' evolve is presented as definitive, when it is ultimately a postulate.

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