Farming and public goods production in Caenorhabditis elegans populations

Abstract

The ecological and evolutionary dynamics of populations are shaped by the strategies they use to produce and use resources. However, our understanding of the interplay between the genetic, behavioral, and environmental factors driving these strategies is limited. Here, we report on a Caenorhabditis elegans-Escherichia coli (worm-bacteria) experimental system in which the worm-foraging behavior leads to a redistribution of the bacterial food source, resulting in a growth advantage for both organisms, similar to that achieved via farming. We show experimentally and theoretically that the increased resource growth represents a public good that can benefit all other consumers, regardless of whether or not they are producers. Mutant worms that cannot farm bacteria benefit from farming by other worms in direct proportion to the fraction of farmers in the worm population. The farming behavior can therefore be exploited if it is associated with either energetic or survival costs. However, when the individuals compete for resources with their own type, these costs can result in an increased population density. Altogether, our findings reveal a previously unrecognized mechanism of public good production resulting from the foraging behavior of C. elegans, which has important population-level consequences. This powerful system may provide broad insight into exploration-exploitation tradeoffs, the resultant ecoevolutionary dynamics, and the underlying genetic and neurobehavioral driving forces of multispecies interactions.

Keywords: farming; foraging behavior; population dynamics; predator–prey; public goods.

Fig. 1.

Redistribution and growth of E. coli bacteria due to locomotion of C. elegans. (A) Trails and patches of bacteria are found away from an initial circular patch (red dashed circle) of bacterial inoculation in which a single worm is placed. The image is taken 4 d after seeding of a bacterial patch with a worm. The bacterial redistribution is due to two main mechanisms: defecation of ingested bacteria (white arrow points to red “feces”) by the worm (B) and entrainment of the bacteria (red) in the wake of the locomoting worm (white arrow shows direction of motion) (C). (D) Worms revisit and colonize the redistributed, growing bacterial patches. Worms disperse bacteria in natural settings such as rotting fruit (E) and soil-like porous medium (F). Arrows indicate initial chunk of worms and bacteria. (Scale bars: A, E, and F, 1 cm; B–D, 500 $\mathrm{\mu }$m.)

Fig. 2.

Farming confers a population growth advantage. (A) N2 worms redistribute bacteria, whereas srf-3 mutants do not. (Scale bar: 1 cm.) (B) Bacterial density on plates (R = 4.5 cm) with N2 (blue circles, n = 4) and srf-3 (red squares, n = 4). (C) The population sizes of N2 worms and the mutant type srf-3 worms 144 h after the start of the experiment for the same initial conditions.

Fig. 3.

Effect of available farming area on the worm population. Worm population as a function of the available dispersal area for the farmer (N2, blue) and nonfarmer (srf-3 mutant, red) worms. (A) Experiments. (B) Numerical results. (A, Inset) Experiments indicating the fold increase in population size of the worms grown on artificially distributed bacterial patches. The data are normalized to a onefold increase in the case of one bacterial patch. Measurements were made 72 h after initialization. The initial amount of bacteria is the same but the patches are distributed either as 1 large patch or the 25 smaller patches formed in a 5 × 5 grid; n = 2–5 for each plate size. (B, Inset) Schematic of the experiment. The bacterial patch is kept constant, whereas the dish size is increased.

Fig. 4.

Redistributed bacteria is a potentially costly public good. (A) Normalized worm population from competition experiments between N2 worms and srf-3 mutant for two different plate sizes (R = 7.5 cm and R = 2.75 cm). The population increase is the ratio of the worm population on the R = 7.5 cm plate to the population on the R = 2.75 cm plate. n = 4 for each experiment. (B) Corresponding data of the competition between farmers and nonfarmers from mathematical model (see SI Appendix for details). (C–E) Mathematical model trajectories of worm population sizes in competitive (solid curves) or clonal (dashed curves) growth conditions. Worm counts are normalized by the initial numbers of that phenotype in the simulation. Competitive dynamics of farmers and nonfarmers (red) when farming inflicts no mortality cost (blue) (C) and some mortality cost (green) (D). (E) Clonal dynamics of farmers with and without mortality cost. The plate size is R = 7.5 cm. All parameters are as in SI Appendix, Table S1.