Article | Published:

Life cycles, fitness decoupling and the evolution of multicellularity

Nature volume 515, pages 7579 (06 November 2014) | Download Citation

Abstract

Cooperation is central to the emergence of multicellular life; however, the means by which the earliest collectives (groups of cells) maintained integrity in the face of destructive cheating types is unclear. One idea posits cheats as a primitive germ line in a life cycle that facilitates collective reproduction. Here we describe an experiment in which simple cooperating lineages of bacteria were propagated under a selective regime that rewarded collective-level persistence. Collectives reproduced via life cycles that either embraced, or purged, cheating types. When embraced, the life cycle alternated between phenotypic states. Selection fostered inception of a developmental switch that underpinned the emergence of collectives whose fitness, during the course of evolution, became decoupled from the fitness of constituent cells. Such development and decoupling did not occur when groups reproduced via a cheat-purging regime. Our findings capture key events in the evolution of Darwinian individuality during the transition from single cells to multicellularity.

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Sequence Read Archive

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All genome data have been deposited into the Sequence Read Archive under accession number SRP047104. P.B.R. will make strains available to qualified recipients.

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Acknowledgements

We thank S. Nestmann for assistance with molecular aspects of the work and for guiding construction of the mutS deletion mutant. We thank E. Libby and Y. Pichugin for discussion, and S. De Monte and P. G. Smith for comments on drafts of the manuscript. We are indebted to PacBio and particularly J. Korlach and Y. Song for genome sequencing. P.B.R. currently holds an International Blaise Pascal Research Chair funded by the French State and the Ile-de-France, managed by the Fondation de l'Ecole Normale Supérieure. The work was directly supported by the Marsden Fund Council from government funding administered by the Royal Society of New Zealand, and in part by grant RFP-12-20 from the Foundational Questions in Evolutionary Biology Fund, by the National Science Foundation under Cooperative Agreement Number DBI-0939454, and by an NSF CAREER Award Grant (DEB0952825).

Author information

Author notes

    • Katrin Hammerschmidt
    •  & Caroline J. Rose

    These authors contributed equally to this work.

Affiliations

  1. New Zealand Institute for Advanced Study and Allan Wilson Centre for Molecular Ecology & Evolution, Massey University, Auckland 0745, New Zealand

    • Katrin Hammerschmidt
    • , Caroline J. Rose
    •  & Paul B. Rainey
  2. Department of Biology and BEACON Center for the Study of Evolution in Action, University of Washington, Seattle, Washington 98195, USA

    • Benjamin Kerr
  3. Max Planck Institute for Evolutionary Biology, Plön 24306, Germany

    • Paul B. Rainey

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Contributions

All authors contributed to the conception and design of the study. K.H. and C.J.R. performed research, undertook data analysis and prepared figures. All authors wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Paul B. Rainey.

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    Supplementary Information

    This file contains a Supplementary Discussion, Supplementary References and Supplementary Table 1.

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https://doi.org/10.1038/nature13884

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