Catecholamine receptor polymorphisms affect decision-making in C. elegans

Innate behaviours are flexible: they change rapidly in response to transient environmental conditions, and are modified slowly by changes in the genome. A classical flexible behaviour is the exploration–exploitation decision, which describes the time at which foraging animals choose to abandon a depleting food supply. We have used quantitative genetic analysis to examine the decision to leave a food patch in Caenorhabditis elegans. Here we show that patch-leaving is a multigenic trait regulated in part by naturally occurring non-coding polymorphisms in tyra-3 (tyramine receptor 3), which encodes a G-protein-coupled catecholamine receptor related to vertebrate adrenergic receptors. tyra-3 acts in sensory neurons that detect environmental cues, suggesting that the internal catecholamines detected by tyra-3 regulate responses to external conditions. These results indicate that genetic variation and environmental cues converge on common circuits to regulate behaviour, and suggest that catecholamines have an ancient role in regulating behavioural decisions.

[1]  Jeremy D. Edwards,et al.  Substitution Mapping of dth1.1, a Flowering-Time Quantitative Trait Locus (QTL) Associated With Transgressive Variation in Rice, Reveals Multiple Sub-QTL , 2006, Genetics.

[2]  Oliver Hobert,et al.  PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. , 2002, BioTechniques.

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

[4]  Paul W. Sternberg,et al.  Acute carbon dioxide avoidance in Caenorhabditis elegans , 2008, Proceedings of the National Academy of Sciences.

[5]  Andrew P Morris,et al.  Genetic dissection of a behavioral quantitative trait locus shows that Rgs2 modulates anxiety in mice , 2004, Nature Genetics.

[6]  S. Harvey.  Non-dauer larval dispersal in Caenorhabditis elegans. , 2009, Journal of experimental zoology. Part B, Molecular and developmental evolution.

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

[8]  T. Roeder.  Tyramine and octopamine: ruling behavior and metabolism. , 2005, Annual review of entomology.

[9]  Y. Kimura,et al.  Starvation Induces cAMP Response Element-Binding Protein-Dependent Gene Expression through Octopamine–Gq Signaling in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[10]  M. Sokolowski,et al.  cGMP-dependent protein kinase as a modifier of behaviour. , 2009, Handbook of experimental pharmacology.

[11]  Barak Cohen,et al.  Gene–Environment Interactions at Nucleotide Resolution , 2010, PLoS genetics.

[12]  Masayoshi Enami,et al.  Reverse genetics. , 2002, Vaccine.

[13]  E. Charnov.  Optimal foraging, the marginal value theorem. , 1976, Theoretical population biology.

[14]  Evan Z. Macosko,et al.  Innate Immunity in Caenorhabditis elegans Is Regulated by Neurons Expressing NPR-1/GPCR , 2008, Science.

[15]  Navin Pokala,et al.  Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases , 2009, Neuron.

[16]  Mario de Bono,et al.  A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans , 2008, Proceedings of the National Academy of Sciences.

[17]  R. Greenspan,et al.  Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. , 1997, Science.

[18]  T. Mackay,et al.  Quantitative Trait Loci for Aggressive Behavior in Drosophila melanogaster , 2009, Genetics.

[19]  Daniel Ramot,et al.  The Parallel Worm Tracker: A Platform for Measuring Average Speed and Drug-Induced Paralysis in Nematodes , 2008, PloS one.

[20]  Mark J Alkema,et al.  Tyramine Functions Independently of Octopamine in the Caenorhabditis elegans Nervous System , 2005, Neuron.

[21]  Mario de Bono,et al.  Behavioral Motifs and Neural Pathways Coordinating O2 Responses and Aggregation in C. elegans , 2006, Current Biology.

[22]  T. Insel,et al.  Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole , 1999, Nature.

[23]  L. Kruglyak,et al.  Recombinational Landscape and Population Genomics of Caenorhabditis elegans , 2009, PLoS genetics.

[24]  T. Wakabayashi,et al.  Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. , 2004, Neuroscience research.

[25]  R. Porter,et al.  DNA transformation. , 1988, Methods in enzymology.

[26]  R. Sommer,et al.  Natural variation in Pristionchus pacificus insect pheromone attraction involves the protein kinase EGL-4 , 2008, Proceedings of the National Academy of Sciences.

[27]  P. Komuniecki,et al.  Tyramine and Octopamine Independently Inhibit Serotonin-Stimulated Aversive Behaviors in Caenorhabditis elegans through Two Novel Amine Receptors , 2007, The Journal of Neuroscience.

[28]  Kaveh Ashrafi,et al.  Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. , 2008, Cell metabolism.

[29]  Cori Bargmann,et al.  Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans , 2007, Proceedings of the National Academy of Sciences.

[30]  M. Chalfie,et al.  Targeted cell killing by reconstituted caspases , 2007, Proceedings of the National Academy of Sciences.

[31]  E. Stone,et al.  The genetics of quantitative traits: challenges and prospects , 2009, Nature Reviews Genetics.

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

[33]  Cori Bargmann,et al.  Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans , 1995, Cell.

[34]  Mark J. Alkema,et al.  A Tyramine-Gated Chloride Channel Coordinates Distinct Motor Programs of a Caenorhabditis elegans Escape Response , 2009, Neuron.

[35]  Leon Avery,et al.  Dietary choice behavior in Caenorhabditis elegans , 2006, Journal of Experimental Biology.

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

[37]  Andrew Fire,et al.  Chapter 19 DNA Transformation , 1995 .

[38]  R. B. Azevedo,et al.  npr-1 Regulates Foraging and Dispersal Strategies in Caenorhabditis elegans , 2008, Current Biology.

[39]  Trudy F. C. Mackay,et al.  Quantitative trait loci in Drosophila , 2001, Nature Reviews Genetics.

[40]  Joel s. Brown,et al.  Foraging : behavior and ecology , 2007 .

[41]  Kazushige Touhara,et al.  Two Chemoreceptors Mediate Developmental Effects of Dauer Pheromone in C. elegans , 2009, Science.

[42]  Leonid Kruglyak,et al.  A Polymorphism in npr-1 Is a Behavioral Determinant of Pathogen Susceptibility in C. elegans , 2009, Science.

[43]  Erik M Jorgensen,et al.  Single-copy insertion of transgenes in Caenorhabditis elegans , 2008, Nature Genetics.

[44]  L. Fiddick,et al.  Evolution and risky decisions , 2000, Trends in Cognitive Sciences.

[45]  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.

[46]  Cori Bargmann,et al.  Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans , 1991, Neuron.

[47]  Jonathan Flint,et al.  Genetic architecture of quantitative traits in mice, flies, and humans. , 2009, Genome research.

[48]  Evan Z. Macosko,et al.  Quantitative Mapping of a Digenic Behavioral Trait Implicates Globin Variation in C. elegans Sensory Behaviors , 2009, Neuron.

[49]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[50]  Evan Z. Macosko,et al.  A huband-spoke circuit drives pheromone attraction and social behaviour in C . elegans , 2009 .

[51]  Hao Wu,et al.  R/qtl: QTL Mapping in Experimental Crosses , 2003, Bioinform..

[52]  W. Frankel,et al.  A major effect QTL determined by multiple genes in epileptic EL mice. , 2000, Genome research.

[53]  Daniel A. Levinthal,et al.  Exploration and Exploitation in Organizational Learning , 2007 .

[54]  Daniel R. Richards,et al.  Dissecting the architecture of a quantitative trait locus in yeast , 2002, Nature.

[55]  Cori Bargmann,et al.  Natural Variation in a Neuropeptide Y Receptor Homolog Modifies Social Behavior and Food Response in C. elegans , 1998, Cell.

[56]  M. Heisenberg,et al.  Octopamine in Male Aggression of Drosophila , 2008, Current Biology.

[57]  A. Sehgal,et al.  Octopamine Regulates Sleep in Drosophila through Protein Kinase A-Dependent Mechanisms , 2008, The Journal of Neuroscience.