Spatial self-organization resolves conflicts between individuality and collective migration

Abstract

Collective behavior can spontaneously emerge when individuals follow common rules of interaction. However, the behavior of each individual differs due to existing genetic and non-genetic variation within the population. It remains unclear how this individuality is managed to achieve collective behavior. We quantify individuality in bands of clonal Escherichia coli cells that migrate collectively along a channel by following a self-generated gradient of attractant. We discover that despite substantial differences in individual chemotactic abilities, the cells are able to migrate as a coherent group by spontaneously sorting themselves within the moving band. This sorting mechanism ensures that differences between individual chemotactic abilities are compensated by differences in the local steepness of the traveling gradient each individual must navigate, and determines the minimum performance required to travel with the band. By resolving conflicts between individuality and collective migration, this mechanism enables populations to maintain advantageous diversity while on the move.

Evolution of specialized microbial cooperation in dynamic fluids

“…Organelles (Kutschera & Niklas, 2005;Siegel, 1960), single (Lewis, 2007) and multi-phenotype (Fu et al, 2018;Koufopanou, 1994) bacterial populations, tissues and organs in multicellular organisms (Carroll, 2001;Hedges, Blair, Venturi, & Shoe, 2004), casts and social classes in colonial animals (Beshers & Fewell, 2001;Smith, Toth, Suarez, & Robinson, 2008), and guilds in ecological communities (Futuyma & Moreno, 1988;May & Seger, 1986;Terborgh, 1986), all fulfil specialized roles that are vital for the functioning of a larger whole. Specialization also gives rise to metabolic interdependencies in microbial populations and can serve as a strong mechanism for community assembly (Zelezniak et al, 2015).…”

“…E. coli can differentiate into transient nongrowing cells and normally growing cells to hedge their bets across different environments (Lewis, 2007). A travelling band of E. coli will exhibit a continuum of navigation styles, each specializing in processing different local conditions while still moving in unison (Fu et al, 2018).…”

Chemotactic behaviour ofEscherichia coliat high cell density

“…Although the principles of chemotactic sensing are fairly well understood for a single cell [28,30], little is known of the effects of physical interactions between cells on chemotaxis, despite their frequent occurrence during self-concentration processes [37][38][39][40][41][42] or high-density collective motility [21,22,26]. Here we used a model system, a suspension of E. coli in a controlled environment, to investigate the effect of collective motion, emerging when cell density increases, on chemotactic sensing.…”

“…Although typically seen as a single-cell behavior, chemotaxis also drives collective behaviors based on chemical interactions, such as autoaggregation [37,38], self-concentration in patches [39,40] and travelling band formation [41,42], where chemotactic response to self-generated gradients of chemoattractants lead to local cell density increases. However, very little is known about how the high-density physical interactions and the resulting collective motion influence the chemotactic navigation of bacteria [43,44]: e.g., would chemotaxis be improved by alignments of convective flows with the gradient [12,44] or compromised by random collisions between cells?…”

Bet-hedging strategies in expanding populations

“…Analyses of 25 phenotypic diversity in motile cells suggest that it also may lead to a selective advantage 26 at a population level [23][24][25]. Although several studies have tackled the problem of how 27 individual variability affects population expansion [6,9,10,26,27,27,28,[28][29][30], 28 systematic and predictive theory is still lacking [22].…”