TY - JOUR
T1 - Eco-evolutionary significance of "loners"
AU - Rossine, Fernando W.
AU - Martinez-Garcia, Ricardo
AU - Sgro, Allyson E.
AU - Gregor, Thomas
AU - Tarnita, Corina E.
N1 - Funding Information:
This work was supported by the Gordon and Betty Moore Foundation (https://www.moore. org) through grant GBMF2550.06, FAPESP (http:// www.fapesp.br/en/) through grants ICTP-SAIFR 2016/01343-7 and Programa Jovens Pesquisadores em Centros Emergentes 2019/ 24433-0, and the Simons Foundation (https://www.simonsfoundation.org) (RMG), NRSA F32 (https://researchtraining.nih.gov/programs/ fellowships/f32) GM103062 (AES), NIH (https:// www.nih.gov) R01 GM098407 (TG), the Alfred P Sloan Foundation (https://sloan.org) and NSF (nsf. gov) EAGER RoL 1838331 (CET). AES was partially supported by a Burroughs Wellcome Fund (https:// www.bwfund.org) Career Award at the Scientific Interface. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Publisher Copyright:
© 2020 Rossine et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2020
Y1 - 2020
N2 - 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.
AB - 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.
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U2 - 10.1371/journal.pbio.3000642
DO - 10.1371/journal.pbio.3000642
M3 - Article
C2 - 32191693
AN - SCOPUS:85082065479
SN - 1544-9173
VL - 18
JO - PLoS biology
JF - PLoS biology
IS - 3
M1 - e3000642
ER -