Dietary choice behavior in Caenorhabditis elegans

SUMMARY Animals have evolved diverse behaviors that serve the purpose of finding food in the environment. We investigated the food seeking strategy of the soil bacteria-eating nematode Caenorhabditis elegans. C. elegans bacterial food varies in quality: some species are easy to eat and support worm growth well, while others do not. We show that worms exhibit dietary choice: they hunt for high quality food and leave hard-to-eat bacteria. This food seeking behavior is enhanced in animals that have already experienced good food. When hunting for good food, worms alternate between two modes of locomotion, known as dwelling: movement with frequent stops and reversals; and roaming: straight rapid movement. On good food, roaming is very rare, while on bad food it is common. Using laser ablations and mutant analysis, we show that the AIY neurons serve to extend roaming periods, and are essential for efficient food seeking.

[1]  B. Roche,et al.  The Behavior of Organisms? , 1997 .

[2]  Rajesh Ranganathan,et al.  C. elegans Locomotory Rate Is Modulated by the Environment through a Dopaminergic Pathway and by Experience through a Serotonergic Pathway , 2000, Neuron.

[3]  P. Sengupta,et al.  Regulation of Body Size and Behavioral State of C. elegans by Sensory Perception and the EGL-4 cGMP-Dependent Protein Kinase , 2002, Neuron.

[4]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[5]  L. Avery,et al.  Food transport in the C. elegans pharynx , 2003, Journal of Experimental Biology.

[6]  L. Avery,et al.  Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. , 1995, Genetics.

[7]  A. V. Maricq,et al.  Dopamine and Glutamate Control Area-Restricted Search Behavior in Caenorhabditis elegans , 2004, The Journal of Neuroscience.

[8]  Cornelia I Bargmann,et al.  Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans , 1995, Neuron.

[9]  S. W. Emmons,et al.  Mate Searching in Caenorhabditis elegans: A Genetic Model for Sex Drive in a Simple Invertebrate , 2004, The Journal of Neuroscience.

[10]  T. B. Osborne,et al.  THE CHOICE BETWEEN ADEQUATE AND INADEQUATE DIETS, AS MADE BY RATS , 1918 .

[11]  Leo X. Liu,et al.  Addresses: 1Laboratoire de Génétique et , 2022 .

[12]  Cori Bargmann,et al.  Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli , 2002, Nature.

[13]  William R Schafer,et al.  eat-2 and eat-18 Are Required for Nicotinic Neurotransmission in the Caenorhabditis elegans Pharynx , 2004, Genetics.

[14]  O. Hobert,et al.  Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. , 2003, Journal of neurobiology.

[15]  G. Ruvkun,et al.  Regulation of Interneuron Function in the C. elegans Thermoregulatory Pathway by the ttx-3 LIM Homeobox Gene , 1997, Neuron.

[16]  M. Yamamoto,et al.  Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. , 2001, The Journal of experimental biology.

[17]  Cori Bargmann,et al.  Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. , 1997, Learning & memory.

[18]  Cori Bargmann,et al.  A Putative Cyclic Nucleotide–Gated Channel Is Required for Sensory Development and Function in C. elegans , 1996, Neuron.

[19]  H. Boyer,et al.  A complementation analysis of the restriction and modification of DNA in Escherichia coli. , 1969, Journal of molecular biology.

[20]  L. Avery,et al.  eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling , 1996, The Journal of cell biology.

[21]  H. Horvitz,et al.  Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. , 1990, The Journal of experimental zoology.

[22]  C. P. Richter Increased salt appetite in adrenalectomized rats. , 1936 .

[23]  A. Sclafani,et al.  Flavor preferences conditioned by intragastric Polycose infusions: A detailed analysis using an electronic esophagus preparation , 1990, Physiology & Behavior.

[24]  R. A. Koelling,et al.  Cues: Their Relative Effectiveness as a Function of the Reinforcer , 1968, Science.

[25]  D. Calcagnetti,et al.  Trends in place preference conditioning with a cross-indexed bibliography; 1957–1991 , 1993, Neuroscience & Biobehavioral Reviews.

[26]  C. P. Richter,et al.  VITAMIN B1 CRAVING IN RATS. , 1937, Science.

[27]  Cornelia I. Bargmann,et al.  Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue , 2004, Nature.

[28]  Wendy S. Schackwitz,et al.  Mutations affecting the chemosensory neurons of Caenorhabditis elegans. , 1995, Genetics.

[29]  P. Young Relative food preferences of the white rat. II. , 1932 .

[30]  S. Lockery,et al.  Mutations in the Caenorhabditis elegans Na,K-ATPase alpha-subunit gene, eat-6, disrupt excitable cell function , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  K. Gengyo-Ando,et al.  HEN-1, a Secretory Protein with an LDL Receptor Motif, Regulates Sensory Integration and Learning in Caenorhabditis elegans , 2002, Cell.

[32]  M. Taussig The Nervous System , 1991 .

[33]  Cori Bargmann,et al.  A circuit for navigation in Caenorhabditis elegans , 2005 .

[34]  S. W. Emmons,et al.  Analysis of the constancy of DNA sequences during development and evolution of the nematode Caenorhabditis elegans. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[35]  E. Fischer Conditioned Reflexes , 1942, American journal of physical medicine.

[36]  K. Nishikawa,et al.  Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. , 1995, Journal of Molecular Biology.

[37]  F. Ausubel,et al.  A simple model host for identifying Gram-positive virulence factors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Sclafani Dietary‐Induced Overeating a , 1989, Annals of the New York Academy of Sciences.

[39]  D. van der Kooy,et al.  Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  I. Mori,et al.  Neural regulation of thermotaxis in Caenorhabditis elegans , 1995, Nature.

[41]  A. Sclafani,et al.  Flavor Preferences Conditioned by Intragastric Nutrient Infusions in Rats fed Chow or a Cafeteria Diet , 1999, Appetite.

[42]  L. Brain The Nervous System , 1963, Nature.

[43]  C. M. Davis SELF SELECTION OF DIET BY NEWLY WEANED INFANTS: AN EXPERIMENTAL STUDY , 1928 .

[44]  L. Avery,et al.  C elegans: a model for exploring the genetics of fat storage. , 2003, Developmental cell.

[45]  E. Capaldi Why We Eat What We Eat: The Psychology of Eating , 2001 .

[46]  P. Eaton,et al.  TEMPERATURE AND THE GROWTH OF HAIR. , 1937, Science.

[47]  C. Spike,et al.  Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. , 1998, Genetics.

[48]  Cori Bargmann,et al.  Odorant-selective genes and neurons mediate olfaction in C. elegans , 1993, Cell.

[49]  Thomas M. Morse,et al.  The Fundamental Role of Pirouettes in Caenorhabditis elegans Chemotaxis , 1999, The Journal of Neuroscience.

[50]  O. Hobert,et al.  A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. , 2001, Development.

[51]  Cori Bargmann,et al.  Laser killing of cells in Caenorhabditis elegans. , 1995, Methods in cell biology.