Automated Detection and Analysis of Foraging Behavior in C. elegans

AbstractForaging strategies must be tuned to the availability and distribution of resources in the environment. This can occur over generations and lead to genetic differences in foraging behavior, or it can occur on shorter time scales within an individual’s life span. Both genetic and experience-based strategies must be implemented by neural circuits that respond to environmental cues and track internal states, and the analysis of such circuits provides insight into the neural basis of complex decision making. In C. elegans, between-strain genetic differences and within-strain plasticity in foraging has been observed. Most individual changes in foraging are short-term, based on experience over several hours. Here, we tested if developmental experience could permanently alter foraging. We found that in wild strains that are normally highly exploratory, early-life starvation leads to “cautious” foraging behavior in which exploration is reduced. We characterize the behavioral bases for these strategies and identify changes in the dynamics of a locomotory circuit involved in navigation. Overall, we show that some C. elegans strains exhibit adaptive tuning of their foraging behavior based on early-life experience, and this is associated with changes in a core navigation circuit.

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Automated detection and analysis of foraging behavior in Caenorhabditis elegans

Journal of Neuroscience Methods ◽

10.1016/j.jneumeth.2008.01.027 ◽

2008 ◽

Vol 171 (1) ◽

pp. 153-164 ◽

Cited By ~ 19

Author(s):

Kuang-Man Huang ◽

Pamela Cosman ◽

William R. Schafer

Keyword(s):

Caenorhabditis Elegans ◽

Foraging Behavior ◽

Automated Detection

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Farming and public goods production in Caenorhabditis elegans populations

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1608961114 ◽

2017 ◽

Vol 114 (9) ◽

pp. 2289-2294 ◽

Cited By ~ 16

Author(s):

Shashi Thutupalli ◽

Sravanti Uppaluri ◽

George W. A. Constable ◽

Simon A. Levin ◽

Howard A. Stone ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Public Good ◽

Foraging Behavior ◽

Evolutionary Dynamics ◽

Driving Forces ◽

Experimental System ◽

Population Level ◽

C Elegans ◽

Exploration Exploitation ◽

Insight Into

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.

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Automated detection and manipulation of sleep in C. elegans reveals depolarization of a sleep-active neuron during mechanical stimulation-induced sleep deprivation

Scientific Reports ◽

10.1038/s41598-018-28095-5 ◽

2018 ◽

Vol 8 (1) ◽

Cited By ~ 9

Author(s):

Jan Spies ◽

Henrik Bringmann

Keyword(s):

Sleep Deprivation ◽

Mechanical Stimulation ◽

Automated Detection ◽

Active Neuron ◽

C Elegans

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Regulatory changes in two chemoreceptor genes contribute to a Caenorhabditis elegans QTL for foraging behavior

eLife ◽

10.7554/elife.21454 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 39

Author(s):

Joshua S Greene ◽

May Dobosiewicz ◽

Rebecca A Butcher ◽

Patrick T McGrath ◽

Cornelia I Bargmann

Keyword(s):

Caenorhabditis Elegans ◽

Foraging Behavior ◽

Sensory Neurons ◽

Exploratory Behavior ◽

Adaptive Variation ◽

C Elegans ◽

Regulatory Changes ◽

Naturally Occurring ◽

Genome Wide ◽

Natural Isolates

Natural isolates of C. elegans differ in their sensitivity to pheromones that inhibit exploratory behavior. Previous studies identified a QTL for pheromone sensitivity that includes alternative alleles of srx-43, a chemoreceptor that inhibits exploration through its activity in ASI sensory neurons. Here we show that the QTL is multigenic and includes alternative alleles of srx-44, a second chemoreceptor gene that modifies pheromone sensitivity. srx-44 either promotes or inhibits exploration depending on its expression in the ASJ or ADL sensory neurons, respectively. Naturally occurring pheromone insensitivity results in part from previously described changes in srx-43 expression levels, and in part from increased srx-44 expression in ASJ, which antagonizes ASI and ADL. Antagonism between the sensory neurons results in cellular epistasis that is reflected in their transcription of insulin genes that regulate exploration. These results and genome-wide evidence suggest that chemoreceptor genes may be preferred sites of adaptive variation in C. elegans.

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Environmental Programming of Adult Foraging Behavior in C. elegans

Current Biology ◽

10.1016/j.cub.2019.07.045 ◽

2019 ◽

Vol 29 (17) ◽

pp. 2867-2879.e4 ◽

Cited By ~ 5

Author(s):

Sreeparna Pradhan ◽

Sabrina Quilez ◽

Kai Homer ◽

Michael Hendricks

Keyword(s):

Foraging Behavior ◽

C Elegans

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Sex-specific, pdfr-1-dependent modulation of pheromone avoidance by food abundance enables flexibility in C. elegans foraging behavior

10.1101/2021.03.16.435685 ◽

2021 ◽

Author(s):

Jintao Luo ◽

Douglas S. Portman

Keyword(s):

Population Density ◽

Foraging Behavior ◽

Internal State ◽

Food Abundance ◽

Wild Type ◽

C Elegans ◽

Biological Sex ◽

Multiple Dimensions ◽

Foraging Decisions ◽

Genetic Mechanisms

To make adaptive feeding and foraging decisions, animals must integrate diverse sensory streams with multiple dimensions of internal state. In C. elegans, foraging and dispersal behaviors are influenced by food abundance, population density, and biological sex, but the neural and genetic mechanisms that integrate these signals are poorly understood. Here, by systematically varying food abundance, we find that chronic avoidance of the population-density pheromone ascr#3 is modulated by food thickness, such that hermaphrodites avoid ascr#3 only when food is scarce. The integration of food and pheromone signals requires the conserved neuropeptide receptor PDFR-1, as pdfr-1 mutant hermaphrodites display strong ascr#3 avoidance even when food is abundant. Conversely, increasing PDFR-1 signaling inhibits ascr#3 aversion when food is sparse, indicating that this signal encodes information about food abundance. In both wild-type and pdfr-1 hermaphrodites, chronic ascr#3 avoidance requires the ASI sensory neurons. In contrast, PDFR-1 acts in interneurons, suggesting that it modulates processing of the ascr#3 signal. Although a sex-shared mechanism mediates ascr#3 avoidance, food thickness modulates this behavior only in hermaphrodites, indicating that PDFR-1 signaling has distinct functions in the two sexes. Supporting the idea that this mechanism modulates foraging behavior, ascr#3 promotes ASI-dependent dispersal of hermaphrodites from food, an effect that is markedly enhanced when food is scarce. Together, these findings identify a neurogenetic mechanism that sex-specifically integrates population and food abundance, two important dimensions of environmental quality, to optimize foraging decisions. Further, they suggest that modulation of attention to sensory signals could be an ancient, conserved function of pdfr-1.

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The glycomes of Caenorhabditis elegans and other model organisms

Biochemical Society Symposium ◽

10.1042/bss0690117 ◽

2002 ◽

Vol 69 ◽

pp. 117-134 ◽

Cited By ~ 47

Author(s):

Stuart M. Haslam ◽

David Gems ◽

Howard R. Morris ◽

Anne Dell

Keyword(s):

Caenorhabditis Elegans ◽

Current Knowledge ◽

Structural Data ◽

Model Organisms ◽

Entire Genome ◽

C Elegans ◽

The Face ◽

Area Of Concern ◽

Nematode Worm

There is no doubt that the immense amount of information that is being generated by the initial sequencing and secondary interrogation of various genomes will change the face of glycobiological research. However, a major area of concern is that detailed structural knowledge of the ultimate products of genes that are identified as being involved in glycoconjugate biosynthesis is still limited. This is illustrated clearly by the nematode worm Caenorhabditis elegans, which was the first multicellular organism to have its entire genome sequenced. To date, only limited structural data on the glycosylated molecules of this organism have been reported. Our laboratory is addressing this problem by performing detailed MS structural characterization of the N-linked glycans of C. elegans; high-mannose structures dominate, with only minor amounts of complex-type structures. Novel, highly fucosylated truncated structures are also present which are difucosylated on the proximal N-acetylglucosamine of the chitobiose core as well as containing unusual Fucα1–2Gal1–2Man as peripheral structures. The implications of these results in terms of the identification of ligands for genomically predicted lectins and potential glycosyltransferases are discussed in this chapter. Current knowledge on the glycomes of other model organisms such as Dictyostelium discoideum, Saccharomyces cerevisiae and Drosophila melanogaster is also discussed briefly.

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