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Emergence of diverse life cycles and life histories at the origin of multicellularity

Nature Ecology & Evolution volume 3, pages 1197–1205 (2019)Cite this article

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Abstract

The evolution of multicellularity has given rise to a remarkable diversity of multicellular life cycles and life histories. Whereas some multicellular organisms are long-lived, grow through cell division, and repeatedly release single-celled propagules (for example, animals), others are short-lived, form by aggregation, and propagate only once, by generating large numbers of solitary cells (for example, cellular slime moulds). There are no systematic studies that explore how diverse multicellular life cycles can come about. Here, we focus on the origin of multicellularity and develop a mechanistic model to examine the primitive life cycles that emerge from a unicellular ancestor when an ancestral gene is co-opted for cell adhesion. Diverse life cycles readily emerge, depending on ecological conditions, group-forming mechanism, and ancestral constraints. Among these life cycles, we recapitulate both extremes of long-lived groups that propagate continuously and short-lived groups that propagate only once, with the latter type of life cycle being particularly favoured when groups can form by aggregation. Our results show how diverse life cycles and life histories can easily emerge at the origin of multicellularity, shaped by ancestral constraints and ecological conditions. Beyond multicellularity, this finding has similar implications for other major transitions, such as the evolution of sociality.

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Fig. 1: Overview of the model.
Fig. 2: Emergence of diverse multicellular life cycles.
Fig. 3: Topologies of evolved gene regulatory networks.
Fig. 4: Emergent multicellular life cycles differ in their life history strategies.
Fig. 5: Coming together facilitates the evolution of novel life cycles.

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Data availability

The study is theoretical; no new empirical data were generated.

Code availability

The simulation code supporting this work is available for download from https://doi.org/10.5281/zenodo.2845406. Pseudocode is available in the Supplementary Methods.

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Acknowledgements

We dedicate this study to the memory of John Tyler Bonner, whose work has been a source of great inspiration. We thank S. De Monte for comments and discussions and the Theoretical Biology & Bioinformatics group at Utrecht University for computing resources. J.v.G. received support from the EMBO Long-Term Fellowship (no. ALTF 1101-2016) and the Marie Sklodowska-Curie Individual Fellowship (no. 742235). C.E.T. acknowledges support from the US National Science Foundation (no. RoL:FELS:EAGER#1838331).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Merlijn Staps & Corina E. Tarnita

  2. Department of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, Switzerland

    Jordi van Gestel

  3. Swiss Institute of Bioinformatics, Lausanne, Switzerland

    Jordi van Gestel

  4. Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland

    Jordi van Gestel

  5. Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Dübendorf, Switzerland

    Jordi van Gestel

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  1. Merlijn Staps
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J.v.G. and C.E.T. conceived the study. All authors developed the model. M.S. performed the computational work and analysed the data. All authors interpreted the results and wrote the manuscript.

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Correspondence to Jordi van Gestel or Corina E. Tarnita.

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Supplementary Methods, Supplementary Analyses and Supplementary Figures 1–9.

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Staps, M., van Gestel, J. & Tarnita, C.E. Emergence of diverse life cycles and life histories at the origin of multicellularity. Nat Ecol Evol 3, 1197–1205 (2019). https://doi.org/10.1038/s41559-019-0940-0

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