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 elegansEscherichia 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 explorationexploitation tradeoffs, the resultant ecoevolutionary dynamics, and the underlying genetic and neurobehavioral driving forces of multispecies interactions.foraging behavior | public goods | predator-prey | population dynamics | farming T he 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 stu...

Disentangling bacterial invasiveness from lethality in an experimental host‐pathogen system

“…These results might lead to novel insight in studies in which various pathogens are screened (e.g., in C. elegans ; Diard et al , ), and contribute to demonstrate that a reductionist approach to infection is possible (Hall et al , ). They also show that C. elegans is an excellent model system for unraveling simple quantitative laws in biology, as already recently proved in other fields such as aging (Stroustrup et al , ) and eco‐evolutionary dynamics (Thutupalli et al , ).…”

From apparent competition to facilitation: Impacts of consumer niche construction on the coexistence and stability of consumer‐resource communities

“…We also assume that the consumer positively affects one of the two resource species only. Note, however, that a consumer may have positive effects on several resources, for example in the cases of nutrient cycling (Cargill & Jefferies, 1984;de Mazancourt et al, 1998) and seed dispersal (Thutupalli et al, 2017) depending on the specialization of the disperser species. Explicit simulations of these more complex (i.e.…”

“…Finally, a predator may help its prey's dispersal and reproduction, for example, seed dispersal linked to granivory (Davidson, 1977), or reduce prey intraspecific competition. The nematode Caenorhabditis elegans for instance transports its prey bacteria and inoculate them to unexploited resource pools (Ingham, Trofymow, Ingham, & Coleman, 1985;Thutupalli et al, 2017).…”

Attraction to pheromones inCaenorhabditis eleganscan be reversed through associative learning

“…However, bacterial food is heterogeneously distributed also at smaller spatial scales, i.e. on the 152 rotting material (30) and worms need to make decisions about how to explore it (31,32), integrating 153 information on food availability and pheromones (22). Pheromones concentrate around food 154 patches that have been discovered, signaling either presence of food, if worms have just started to 155 consume the food patch, or absence of food, if the food patch has been exploited.…”

“…Although further investigation is 173 needed to ascertain the impact of such processes in the wild, these results suggests that plasticity in 174 the behavioral response to pheromones may be a further adaptation to exploit ephemeral food 175 sources in a most efficient manner. Intriguingly, C. elegans individuals engage in a primitive form 176 of farming by redistributing bacteria while foraging (31), and having navigational cues that help 177…”