The cost of being big: Local competition, importance of dispersal, and experimental evolution of reversal to unicellularity

María Rebolleda-Gómez, Michael Travisano

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

Abstract

Multicellularity provides multiple benefits. Nonetheless, unicellularity is ubiquitous, and there have been multiple cases of evolutionary reversal to a unicellular organization. In this article, we explore some of the costs of multicellularity as well as the possibility and dynamics of evolutionary reversals to unicellularity. We hypothesize that recently evolved multicellular organisms would face a high cost of increased competition for local resources in spatially structured environments because of larger size and increased cell densities. To test this hypothesis we conducted competition assays, computer simulations, and selection experiments using isolates of Saccharomyces cerevisiae that recently evolved multicellularity. In well-mixed environments, multicellular isolates had lower growth rates relative to their unicellular ancestor because of limitations of space and resource acquisition. In structured environments with localized resources, cells in both multicellular and unicellular isolates grew at a similar rate. Despite similar growth, higher local density of cells in multicellular groups led to increased competition and higher fitness costs in spatially structured environments. In structured environments all of the multicellular isolates rapidly evolved a predominantly unicellular life cycle, while in well-mixed environments reversal was more gradual. Taken together, these results suggest that a lack of dispersal, leading to higher local competition, might have been one of the main constraints in the evolution of early multicellular forms.

Original languageEnglish (US)
Pages (from-to)731-744
Number of pages14
JournalAmerican Naturalist
Volume192
Issue number6
DOIs
StatePublished - Dec 1 2018

Bibliographical note

Funding Information:
We thank Allison Shaw and everyone at the University of Minnesota biological theory group for advice on simulations. Emilie Snell-Rood, Ruth Shaw, Vaughn Cooper, Ford Denison, Jake Grossman, Amy Kendig, Melanie Bowman, and two reviewers all provided useful feedback and thoughtful comments. We especially acknowledge all the feedback provided by editors Judith L. Bronstein and Ben M. Bolker. This work was developed as part of M.R.-G.’s doctoral dissertation with support from the Interdisciplinary Center for the Study of Global Change as well as the Interdisciplinary Doctoral Fellowship and Doctoral Dissertation Fellowship from the graduate school at the University of Minnesota. We thank Will Harcombe for the use of his plate reader and thoughtful discussions. M.T. is funded by the John Templeton Foundation, and M.R.-G. had funding from an ICGC fellowship at the University of Minnesota. This work was supported by National Science Foundation grant DEB-1051115. We have no conflicting interests to declare.

Publisher Copyright:
© 2018 by The University of Chicago. All rights reserved.

Keywords

  • Cooperation
  • Dispersal
  • Experimental evolution
  • Local competition
  • Multicellularity
  • Resource limitation

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