Eco-evolutionary significance of “loners”

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 stagearise 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.

Social Conflicts in <em>Dictyostelium discoideum</em> : A Matter of Scales

“…The potential relevance of non-aggregated cells has been supported by experimental observations both on lab and wild strains. Different studies reported that a sizeable fraction of cells is invariably found outside aggregates, and that these cells are able to start vegetative growth when nutrients become available (Dubravcic et al, 2014;Tarnita et al, 2015;Rossine et al, 2020). The partition of a population in loner and aggregated components was modelled as the consequence of a cell-level stochastic choice, where the genotype determines the probability of staying alone (Dubravcic et al, 2014;Tarnita et al, 2015;Martínez-García & Tarnita, 2016).…”

“…As discussed earlier in this section, a possible source of indirect effects on the proportion of spores produced by one strain in a chimera is the partition between aggregated and non-aggregated cells. When exploring the mechanistic bases of this partitioning, the probability of being a loner was found to depend, other than on the genotype, on cell density and environmental factors such as the hardness of the agar substrate (Rossine et al, 2020). Such dependence on both the biotic and abiotic context was explained by a mathematical model where the cell decision to aggregate is stochastic and conditional on a locally established quorum.…”

“…For instance, strains that tend to aggregate less can still contribute to aggregation of another strain, and they do so more efficiently when they are more dense. The end result of cell self-organization in groups is then frequency dependence, which can sustain coexistence of multiple strains over evolutionary times (Rossine et al, 2020).…”

“…In Dictyostelium, genetically homogeneous populations produce both spores and stalk. Stochastic choices are thought to be involved at the onset of aggregation, in establishing aggregation centers (Gregor et al, 2010); during aggregation, in the decisions whether to follow the cAMP gradient (Rossine et al, 2020); and even during development, in mixing of pre-spore and pre-stalk cells within a slug (Weijer, 1999). On the other hand, phenotypic heterogeneity in isogenic populations can also result from deterministic sources, such as the distribution of cell cycle phase in asynchronously dividing cultures (Jang & Gomer, 2011;Gruenheit et al, 2018) or the spatial distribution of cell density (Vidal-Henriquez & Gholami, 2019).…”

Species exclusion and coexistence in a noisy voter model with a competition-colonization tradeoff

“…Studying the balance between species competitive and dispersal abilities is fundamental to understanding the role of space in maintaining biodiversity [1][2][3][4][5][6]. Competition-dispersal (or competition-colonization) tradeoffs have primarily been invoked to explain the structure of plant communities [7][8][9][10], but have also been measured in virus [11], insects [12], bacteria [13,14], rotifers and protozoan [15], and slime molds [16][17][18][19] among other lineages. A key result is that species that are weaker competitors may persist in the community because their enhanced dispersal, either in distance or rate, allows them to colonize empty patches before the stronger competitor arrives [2].…”