Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America.
ICTP-South American Institute for Fundamental Research and Instituto de Fisica Teorica da UNESP, Sao Paulo, SP Brazil.
PLoS Biol. 2020 Mar 19;18(3):e3000642. doi: 10.1371/journal.pbio.3000642. eCollection 2020 Mar.
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.
孤独者——与协调的大多数人不同步的个体——在自然界中经常出现。孤独者是大规模协调尝试的偶然副产品，还是生命史策略的马赛克的一部分？在这里，我们提供了模型社会变形虫盘基网柄菌中孤独行为的自然发生遗传变异的经验证据。我们提出，盘基网柄菌孤独者——不加入多细胞生命阶段的细胞——来自于一个动态的种群分割过程，是每个细胞做出随机、基于信号的决策的结果。我们发现有证据表明，这种不完全同步的多细胞发育受到非生物（环境渗透性）和生物（信号）因素的影响。最后，我们从理论上预测，当一对具有不同分割行为的菌株共同聚集时，跨信号会影响时空尺度上的粘液霉菌多样性。我们的研究结果表明，孤独者对于理解集体和社会行为、多细胞发育以及盘基网柄菌的生态动态可能至关重要。更广泛地说，在整个分类群中，集体行为的不协调可能是适应性的，因为它可以使生命史策略多样化。
