Significance The population dynamics of species arise from individual-level inter- and intraspecies interactions, driven by genetic and neurobehavioral factors. However, linking ecological and evolutionary dynamics to underlying mechanisms represents a major challenge, largely due to experimental intractability. Here, we study the population dynamics of a predator–prey system comprising the nematode worm Caenorhabditis elegans and bacteria Escherichia coli. We find that the worms engage in a form of primitive agriculture, driven by their foraging behavior, by redistributing their bacterial food source, which subsequently grows. Our findings have ecoevolutionary consequences that are broadly applicable not only to worm–bacterial dynamics but also for diverse situations such as the spread of epidemics, foraging behavior, seed dispersal, and the organisms’ engineering of their habitat.

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.

The fitness of an organism is affected by its strategies to produce, explore, and exploit resources (1, 2). These strategies are influenced, in large part, by interdependencies among organisms, such as competition, predation (3, 4), mutualism (5⇓–7), or the production of public good resources (8⇓–10). Despite the wide prevalence of such interactions in nature as well as numerous theoretical and empirical studies, we are still limited in our mechanistic understanding of the interplay between different survival strategies, the resultant evolutionary dynamics and the underlying genetic, neurobehavioral, and ecological driving forces. In this pursuit, model systems in the laboratory have served as a useful bridge between the complexity of nature and the simplifications inherent in theoretical investigations. Such model systems have predominantly been either microbial (11, 12) or higher organisms, such as primates and humans (13⇓⇓–16). Microbial systems are very convenient due to their genetic tractability and short generation times but are limited in the space of behavioral traits they exhibit. At the other extreme, higher organisms exhibit rich neurobehavioral and genetic traits, but they are difficult to experimentally manipulate and generation times are very long.

Recently, organisms such as the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster have been increasingly used in evolutionary and behavioral studies (17⇓–19). These organisms demonstrate complex behavior and yet retain experimental tractability due to their extensive development as model systems in neurobiology and genetics. The C. elegans worms, in particular, are amenable to experimental tracking of large populations and multiple generations at high resolution (20⇓⇓–23), which has made them one of the most widely used model organisms in behavioral, genetic, and neurobiological studies.

The ecological and evolutionary backgrounds of C. elegans, however, have remained unclear for a long time, and only recently have insights into the organism’s natural habitat begun to be uncovered. Contrary to the common perception that it is a soil nematode, C. elegans is primarily a colonizer of microbe-rich habitats including decaying organic matter where resources are finite and are quickly depleted (24, 25). C. elegans populations are characterized by a rich set of ecological dynamics: (i) a boom and bust population dynamics due to ephemeral resources (26), self-fertilization (27), and dauer developmental stages (28); (ii) dispersal and migration by various means (26); (iii) competition (26, 29, 30); and even (iv) host–microbe interactions (24, 25, 30, 31). Such a lifestyle is naturally tied with the movement patterns of the worms through the complex environments where they dwell. In the laboratory, the foraging strategies of C. elegans, which are a key determinant of their fitness, are influenced both by the distribution and quality of resources (32) and by the presence of competitors (33), whether they are of the same or different genotypes, a scenario that likely results from local genetic diversity induced by worm movement (25). Therefore, C. elegans is an ideal model organism to study the interplay between ecology (resource distribution, inter and intraspecies interactions) and behavior (e.g., foraging strategies, public goods production) and to explore the genetic and neural circuits responsible for integrating ecological information. However, the potential for exploring these areas using C. elegans populations remains largely untapped.

Here, we use the C. elegans–bacteria (E. coli) system to study the emergent population dynamics of each species. C. elegans feed on bacteria and persistently forage for new bacterial food sources. Using both experimental and theoretical approaches, we uncover a relationship between foraging and a hitherto unrecognized mechanism of public goods production. This production of public goods leads to a long-term fitness advantage for both the worms and the bacteria, but one that can easily be exploited by nonproducing types.

Conclusions We have shown that C. elegans worms engage in a primitive form of farming of the bacterial resource that they feed on. The farming is brought about by the redistribution of bacteria by foraging worms, resulting in an increased amount of bacteria, which can be exploited by nonproducers. This form of public goods production, which may be incidental to the foraging behavior of the worms, is qualitatively different from situations in which the good production is associated only with the explicit metabolic cost of chemical synthesis of the good, a mechanism often at play in microbial systems (6, 8⇓–10), which lack complex behaviors. In contrast, the mechanism of public goods production that we describe here could be associated with neurobehavioral traits, such as exploration–exploitation strategies (18, 19, 29, 40⇓–42) or the use of spatial memory (42, 43), in addition to potential metabolic costs associated with carrying the bacteria (37, 38). Moreover, C. elegans also appear to be capable of dispersing Dictyostelium discoideum spores (44), another food source; given that D. discoideum themselves farm bacteria (7), we anticipate a rich set of multitrophic level dynamics and niche partitioning to emerge in multispecies interactions involving the kind of effects that we have uncovered here. More specifically, these previously unobserved effects of worm-foraging behavior are likely to have significant consequences for experimental work involving C. elegans populations; even the most routine aspects of worm maintenance in the laboratory are likely to be affected by these dynamics. The dynamics in our system have a striking similarity to a range of spreading processes in nature such as the dispersal of seeds or the carrying of commensal infectious agents by mobile vectors (14, 45, 46). Empirical data in these cases are limited, and even when available, the data are observational rather than experimental. Moreover, in processes such as the dispersal of seeds (46), the benefit to the disperser likely occurs on a much longer time scale compared with the benefit accrued by the dispersed. In contrast, the impact of the bacterial redistribution reported here occurs on a fast time scale, with effects similar to those of farming in other organisms (7, 47⇓⇓⇓–51). This characteristic allows for experimental and theoretical investigations into the role of farming in driving and shaping the evolutionary dynamics of foraging. In addition, the microbial populations on which the worms feed are redistributed through the ecological landscape, which affects the composition of microbial communities and their relationships and interactions. Altogether, these effects will shape the local microbial and worm ecologies in ways that significantly affect their dynamics. Although further investigations are needed to determine the impact of such dynamics in the wild, this incidental dropping of “resource seeds” is remarkably similar to the early stages of human agriculture during which “… people who gathered [wheat] grains carried them back to their temporary campsites for processing…some of them inevitably fell on the way to the campsite and were lost. Over time, more and more wheat grew along favorite human trails and near campsites” (52).

Materials and Methods C. elegans Strains and Culture. N2 Bristol (laboratory wild type) and AT10 (srf-3 (yj10)) (mutant type) were obtained from the Caenorhabditis Genetics Center (CGC) and maintained on standard nematode growth medium (NGM) plates supplemented with ampicillin and seeded with OP50-GFP E. coli (GFP plasmid pFVP25.1 with ampicillin resistance) also obtained from the CGC. For competition experiments, CPB089 ( Pdao 5 : dao 5 : GFP ), with the same brood size as N2 worms, generated in house by CRISPR technology, was used as a substitute. For all experiments, 20 μ L of bacteria at OD 600 = 2.0 per worm were seeded on NGM plates of the appropriate size. Worms were age-synchronized by bleaching and individual larval stage 4 (L4) worms were placed onto dishes of the appropriate size. Brood size was quantified by counting the number of embryos laid in 24-h intervals by age-synchronized worms on standard NGM plates, at which time worms were moved to a fresh dish. OD 600 shown in Fig. 2 was measured using a NanoDrop (ThermoScientific) by washing each plate with the same volume of M9 buffer. Imaging. To image entire Petri dish surfaces such as in Fig. 1A, we used a desktop flatbed scanner (Epson V700) custom-fitted with a blue light LED strip to excite fluorescence emission in the OP50-GFP E. coli and a corresponding photographic emission filter (Kodak) to record the image. Flow Cytometry. Individual plates were carefully washed with M9 buffer and inspected to collect all worms. Worm samples were washed to remove bacteria and then transferred to a Complex Object Parametric Analyzer and Sorter Biosort (Union Biometrica) sample cup at a dilution of approximately one nematode per microliter in M9 buffer. To distinguish N2 and mutant worms, fluorescent gates were determined by running fluorescent worms and nonfluorescent worms separately. All data are shown as means F0B1 SEM.

Acknowledgments We thank Christina DeCoste (Princeton Flow Cytometry Resource Facility) for invaluable assistance with the COPAS Biosort. We are grateful to Paulina Orillac for help with the initial setup of the experiments. We thank Mochi Liu for help with worm tracking and Bindu Madhav U for help with worm counting. Worm and bacterial strains were obtained from the CGC, which is funded by NIH Office of Research Infrastructure Programs Grant P40 OD010440. S.T. acknowledges the Human Frontier Science Program (Cross Disciplinary Fellowship) for funding. C.P.B. and S.U. acknowledge support from NIH Director’s New Innovator Award 1DP2GM105437-01 and Searle Scholars Program Grant 12-SSP-217. S.L. was supported by Simons Foundation Grant 395890.