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Eco-evolutionary significance of “loners”

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  • Fernando W Rossine
  • Ricardo Martinez-Garcia
  • Allyson E Sgro
  • Thomas Gregor
  • Corina E Tarnita

Abstract

Loners—individuals out of sync with a coordinated majority—occur frequently in nature. Are loners incidental byproducts of large-scale coordination attempts, or are they part of a mosaic of life-history strategies? Here, we provide empirical evidence of naturally occurring heritable variation in loner behavior in the model social amoeba Dictyostelium discoideum. We propose that Dictyostelium loners—cells that do not join the multicellular life stage—arise from a dynamic population-partitioning process, the result of each cell making a stochastic, signal-based decision. We find evidence that this imperfectly synchronized multicellular development is affected by both abiotic (environmental porosity) and biotic (signaling) factors. Finally, we predict theoretically that when a pair of strains differing in their partitioning behavior coaggregate, cross-signaling impacts slime-mold diversity across spatiotemporal scales. Our findings suggest that loners could be critical to understanding collective and social behaviors, multicellular development, and ecological dynamics in D. discoideum. More broadly, across taxa, imperfect coordination of collective behaviors might be adaptive by enabling diversification of life-history strategies.Loners (individuals out of sync with a coordinated majority) occur frequently in nature and are generally assumed to be incidental by-products of imperfect coordination attempts. Experimental and theoretical work on the slime mold Dictyostelium discoideum suggests that "lonerism" might actually be an alternative life-history strategy.

Suggested Citation

  • Fernando W Rossine & Ricardo Martinez-Garcia & Allyson E Sgro & Thomas Gregor & Corina E Tarnita, 2020. "Eco-evolutionary significance of “loners”," PLOS Biology, Public Library of Science, vol. 18(3), pages 1-27, March.
  • Handle: RePEc:plo:pbio00:3000642
    DOI: 10.1371/journal.pbio.3000642
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    References listed on IDEAS

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    1. Satoshi Sawai & Peter A. Thomason & Edward C. Cox, 2005. "An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations," Nature, Nature, vol. 433(7023), pages 323-326, January.
    2. Joan E. Strassmann & Yong Zhu & David C. Queller, 2000. "Altruism and social cheating in the social amoeba Dictyostelium discoideum," Nature, Nature, vol. 408(6815), pages 965-967, December.
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