npr-1 Regulates Foraging and Dispersal Strategies in Caenorhabditis elegans

Abstract

Wild isolates of Caenorhabditis elegans differ in their tendency to aggregate on food [1, 2]. Most quantitative variation in this behavior is explained by a polymorphism at a single amino acid in the G protein-coupled receptor NPR-1: gregarious strains carry the 215F allele, and solitary strains carry the 215V allele [2]. Although npr-1 regulates a behavioral syndrome with potential adaptive implications, the evolutionary causes and consequences of this natural polymorphism remain unclear. Here we show that npr-1 regulates two behaviors that can promote coexistence of the two alleles. First, gregarious and solitary worms differ in their responses to food such that they can partition a single, continuous patch of food. Second, gregarious worms disperse more readily from patch to patch than do solitary worms, which can cause partitioning of a fragmented resource. The dispersal propensity of both gregarious and solitary worms increases with density. npr-1-dependent dispersal is independent of aggregation and could be part of a food-searching strategy. The gregarious allele is favored in a fragmented relative to a continuous food environment in competition experiments. We conclude that the npr-1 polymorphism could be maintained by a trade-off between dispersal and competitive ability.

Dynamic switching between escape and avoidance regimes reduces Caenorhabditis elegans exposure to noxious heat

“…By this mean, worms favour efficient heat avoidance mechanisms when they are within innocuous temperatures and favour efficient escape mechanisms when they are exposed to noxious heat. This behavioural transition presents some similarities with the local search/dispersal behavioural switch observed following food deprivation 33 and to the dwelling/roaming switches regulated by the quality of food and associated with optimal foraging strategies [34][35][36] . Thus, changing the behavioural rules according to environmental inputs is not only important to improve foraging and exploratory behaviours, but also help minimizing the exposure to noxious heat.…”

MainstreamingCaenorhabditis elegansin experimental evolution

“…By competing in a patchy environment, the experiments showed that environmental variation can favour the evolution of increased dispersal tendencies and that alternative dispersal strategies can coexist under intermediate rates of environmental disturbance [56,57]. Fragmented environments have also been used to test hypotheses about balancing selection for the maintenance of genetic variation within a population, specifically associated with genetic control of feeding strategies [33]. While Petri dishes provide a relatively uniform environment, imposing physical barriers to dispersal has allowed study of dispersal propensity [52] and construction of artificial dirt permits worms to perform behaviour in a more realistic three-dimensional environment rspb.royalsocietypublishing.org Proc.…”

Genetic variation in aggregation behaviour and interacting phenotypes in Drosophila

“…Solitary strains tend to forage evenly throughout the resource whereas gregarious strains tend to forage on the periphery of the resource [17]. When the two phenotypes are mixed, each keeps its own foraging pattern without being affected by interactions with the other [17]. In other situations, phenotypes can interact, with the behaviour of an individual influenced both by genetics and by the phenotype of other individuals in the population.…”

“…In the nematode Caenorhabditis elegans there is a natural variant, linked to the expression of the npr-1 gene, that exhibits either solitary or gregarious patterns of foraging [16]. Solitary strains tend to forage evenly throughout the resource whereas gregarious strains tend to forage on the periphery of the resource [17]. When the two phenotypes are mixed, each keeps its own foraging pattern without being affected by interactions with the other [17].…”