Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila.

Like other ectotherms, the roundworm Caenorhabditis elegans and the fruit fly Drosophila melanogaster rely on behavioral strategies to stabilize their body temperature. Both animals use specialized sensory neurons to detect small changes in temperature, and the activity of these thermosensors governs the neural circuits that control migration and accumulation at preferred temperatures. Despite these similarities, the underlying molecular, neuronal, and computational mechanisms responsible for thermotaxis are distinct in these organisms. Here, we discuss the role of thermosensation in the development and survival of C. elegans and Drosophila, and review the behavioral strategies, neuronal circuits, and molecular networks responsible for thermotaxis behavior.

[1]  The Temperature Preferendum of Certain Insects , 1941 .

[2]  C S Pittendrigh,et al.  ON TEMPERATURE INDEPENDENCE IN THE CLOCK SYSTEM CONTROLLING EMERGENCE TIME IN DROSOPHILA. , 1954, Proceedings of the National Academy of Sciences of the United States of America.

[3]  T. Bullock,et al.  Properties of an infra‐red receptor , 1956, The Journal of physiology.

[4]  J. W. Hastings,et al.  ON THE MECHANISM OF TEMPERATURE INDEPENDENCE IN A BIOLOGICAL CLOCK. , 1957, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Shaw,et al.  Temperature and Life-Span in Poikilothermous Animals , 1962, Nature.

[6]  C. Barlow,et al.  Population Growth of Drosophila melanogaster (Diptera: Drosophilidae) at Constant and Alternating Temperatures , 1972 .

[7]  H. Hensel,et al.  Neural processes in thermoregulation. , 1973, Physiological reviews.

[8]  R. L. Russell,et al.  Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. , 1975, Genetics.

[9]  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.

[10]  M. Klass,et al.  Aging in the nematode Caenorhabditis elegans: Major biological and environmental factors influencing life span , 1977, Mechanisms of Ageing and Development.

[11]  D. Riddle,et al.  A pheromone influences larval development in the nematode Caenorhabditis elegans. , 1982, Science.

[12]  R. Hosono,et al.  Life span of the wild and mutant nematode Caenorhabditis elegans Effects of Sex, Sterilization, and Temperature , 1982, Experimental Gerontology.

[13]  D L Riddle,et al.  The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. , 1984, Developmental biology.

[14]  D. Riddle,et al.  A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Robert D. Stevenson,et al.  The Relative Importance of Behavioral and Physiological Adjustments Controlling Body Temperature in Terrestrial Ectotherms , 1985, The American Naturalist.

[16]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  E Simon,et al.  Central and peripheral thermal control of effectors in homeothermic temperature regulation. , 1986, Physiological reviews.

[18]  J. N. Thomson,et al.  Mutant sensory cilia in the nematode Caenorhabditis elegans. , 1986, Developmental biology.

[19]  B. T. Bloomquist,et al.  Isolation of a putative phospholipase c gene of drosophila, norpA, and its role in phototransduction , 1988, Cell.

[20]  A. F. Bennett Thermal dependence of locomotor capacity. , 1990, The American journal of physiology.

[21]  R. Hardie,et al.  The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors , 1992, Neuron.

[22]  Bernd Heinrich,et al.  The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation , 1993 .

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

[24]  W. Stark,et al.  Phospholipase C Rescues Visual Defect in norpA Mutant of Drosophila melanogaster(*) , 1995, The Journal of Biological Chemistry.

[25]  Monica Driscoll,et al.  Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor , 1995, Nature.

[26]  J. Kaplan,et al.  Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor , 1995, Nature.

[27]  S. Benzer,et al.  Behavioral genetics of thermosensation and hygrosensation in Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[29]  C. Zuker,et al.  The Drosophila Light-Activated Conductance Is Composed of the Two Channels TRP and TRPL , 1996, Cell.

[30]  Ikue Mori,et al.  Mutations in a Cyclic Nucleotide–Gated Channel Lead to Abnormal Thermosensation and Chemosensation in C. elegans , 1996, Neuron.

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

[32]  I. Mori Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. , 1999, Annual review of genetics.

[33]  Cori Bargmann,et al.  Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells , 1999, Brain Research.

[34]  H. Horvitz,et al.  EAT-4, a Homolog of a Mammalian Sodium-Dependent Inorganic Phosphate Cotransporter, Is Necessary for Glutamatergic Neurotransmission in Caenorhabditis elegans , 1999, The Journal of Neuroscience.

[35]  A. Hart,et al.  Neuropeptide Gene Families in the Nematode Caenorhabditis elegans a , 1999, Annals of the New York Academy of Sciences.

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

[37]  G. Ruvkun,et al.  A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  D L Riddle,et al.  daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. , 2000, Genes & development.

[39]  J. Thomas,et al.  Dauer formation induced by high temperatures in Caenorhabditis elegans. , 2000, Genetics.

[40]  J. Satterlee,et al.  Specification of Thermosensory Neuron Fate in C. elegans Requires ttx-1, a Homolog of otd/Otx , 2001, Neuron.

[41]  V. Rottiers,et al.  A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. , 2001, Developmental cell.

[42]  Edouard De Castro,et al.  Ca2+ Signaling via the Neuronal Calcium Sensor-1 Regulates Associative Learning and Memory in C. elegans , 2001, Neuron.

[43]  A. Hart,et al.  Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Donald L Riddle,et al.  DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. , 2002, Development.

[45]  Aravinthan D. T. Samuel,et al.  Thermotaxis in Caenorhabditis elegans Analyzed by Measuring Responses to Defined Thermal Stimuli , 2002, The Journal of Neuroscience.

[46]  I. Mori,et al.  Negative Regulation and Gain Control of Sensory Neurons by the C. elegans Calcineurin TAX-6 , 2002, Neuron.

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

[48]  G. S. Bakken,et al.  Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes , 2003, Journal of Experimental Biology.

[49]  Hatim A. Zariwala,et al.  Step Response Analysis of Thermotaxis in Caenorhabditis elegans , 2003, The Journal of Neuroscience.

[50]  Miriam B Goodman,et al.  Transducing touch in Caenorhabditis elegans. , 2003, Annual review of physiology.

[51]  Gilles Laurent,et al.  painless, a Drosophila Gene Essential for Nociception , 2003, Cell.

[52]  Lei Liu,et al.  Identification and function of thermosensory neurons in Drosophila larvae , 2003, Nature Neuroscience.

[53]  Raymond B Huey,et al.  Behavioral Drive versus Behavioral Inertia in Evolution: A Null Model Approach , 2003, The American Naturalist.

[54]  Y. Ohshima,et al.  Distribution and movement of Caenorhabditis elegans on a thermal gradient , 2003, Journal of Experimental Biology.

[55]  A. Patapoutian,et al.  Ion channels: Opposite thermosensor in fruitfly and mouse , 2003, Nature.

[56]  Aravinthan D. T. Samuel,et al.  Identification of Thermosensory and Olfactory Neuron-Specific Genes via Expression Profiling of Single Neuron Types , 2004, Current Biology.

[57]  A. Antebi,et al.  Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues , 2004, Development.

[58]  M. Thomsen,et al.  Über das Thermopräferendum der Larven einiger Fliegenarten , 2004, Zeitschrift für vergleichende Physiologie.

[59]  Ryuzo Shingai,et al.  Neurons regulating the duration of forward locomotion in Caenorhabditis elegans , 2004, Neuroscience Research.

[60]  M. Tominaga,et al.  Thermosensation and pain. , 2004, Journal of neurobiology.

[61]  R. Bijlsma,et al.  Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding , 2004, Heredity.

[62]  Koutarou D. Kimura,et al.  The C. elegans Thermosensory Neuron AFD Responds to Warming , 2004, Current Biology.

[63]  David B. Dusenbery,et al.  Thermal limits and chemotaxis in mutants of the nematodeCaenorhabditis elegans defective in thermotaxis , 1980, Journal of comparative physiology.

[64]  O. Hobert,et al.  Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. , 2004, Developmental cell.

[65]  G. Ruvkun,et al.  Intercellular signaling of reproductive development by the C. elegans DAF-9 cytochrome P450 , 2004, Development.

[66]  Koutarou D. Kimura,et al.  Genetic Control of Temperature Preference in the Nematode Caenorhabditis elegans , 2005, Genetics.

[67]  L. Leon The Use of Gene Knockout Mice in Thermoregulation Studies , 2005 .

[68]  Shin Murakami,et al.  Aging-Dependent and -Independent Modulation of Associative Learning Behavior by Insulin/Insulin-Like Growth Factor-1 Signal in Caenorhabditis elegans , 2005, Journal of Neuroscience.

[69]  S. N. Fry,et al.  The aerodynamics of hovering flight in Drosophila , 2005, Journal of Experimental Biology.

[70]  B. Kaang,et al.  Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster , 2005, Nature Genetics.

[71]  A. Hoffmann,et al.  The effects of acclimation and rearing conditions on the response of tropical and temperate populations ofDrosophila melanogaster andD. simulans to a temperature gradient (Diptera: Drosophilidae) , 1994, Journal of Insect Behavior.

[72]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

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

[74]  Weontae Lee,et al.  Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone , 2005, Nature.

[75]  Koutarou D. Kimura,et al.  Diverse regulation of sensory signaling by C. elegans nPKC‐epsilon/eta TTX‐4 , 2005, The EMBO journal.

[76]  I. Mori,et al.  Molecular Physiology of the Neural Circuit for Calcineurin-Dependent Associative Learning in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[77]  Damon A. Clark,et al.  The AFD Sensory Neurons Encode Multiple Functions Underlying Thermotactic Behavior in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[78]  Damon A. Clark,et al.  Sensorimotor control during isothermal tracking in Caenorhabditis elegans , 2006, Journal of Experimental Biology.

[79]  Aravinthan D. T. Samuel,et al.  The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation , 2006, BMC Neuroscience.

[80]  Jaeseob Kim,et al.  Histamine and Its Receptors Modulate Temperature-Preference Behaviors in Drosophila , 2006, The Journal of Neuroscience.

[81]  Y. Ye,et al.  Thermal nociception in adult Drosophila: behavioral characterization and the role of the painless gene , 2006, Genes, brain, and behavior.

[82]  Hitoshi Inada,et al.  Identification of Guanylyl Cyclases That Function in Thermosensory Neurons of Caenorhabditis elegans , 2006, Genetics.

[83]  Cori Bargmann Chemosensation in C. elegans. , 2006, WormBook : the online review of C. elegans biology.

[84]  Damon A. Clark,et al.  A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans , 2006, Nature Neuroscience.

[85]  A. Patapoutian,et al.  Trp ion channels and temperature sensation. , 2006, Annual review of neuroscience.

[86]  Koutarou D. Kimura,et al.  Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. , 2006, Genes & development.

[87]  I. Mori,et al.  Quantitative analysis of thermotaxis in the nematode Caenorhabditis elegans , 2006, Journal of Neuroscience Methods.

[88]  D. Mangelsdorf,et al.  Identification of Ligands for DAF-12 that Govern Dauer Formation and Reproduction in C. elegans , 2006, Cell.

[89]  K. Yau,et al.  Phototransduction in mouse rods and cones , 2007, Pflügers Archiv - European Journal of Physiology.

[90]  Raphaelle Winsky-Sommerer,et al.  Transgenic Mice with a Reduced Core Body Temperature Have an Increased Life Span , 2006, Science.

[91]  Aravinthan D. T. Samuel,et al.  Short-term adaptation and temporal processing in the cryophilic response of Caenorhabditis elegans. , 2007, Journal of neurophysiology.

[92]  Sreekanth H. Chalasani,et al.  Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans , 2007, Nature.

[93]  Steven J. M. Jones,et al.  The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. , 2007, Genes & development.

[94]  S. Harvey,et al.  Thermal variation reveals natural variation between isolates of Caenorhabditis elegans. , 2007, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[95]  Raymond B Huey,et al.  Thermal preference of Caenorhabditis elegans: a null model and empirical tests , 2007, Journal of Experimental Biology.

[96]  Damon A. Clark,et al.  Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients , 2007, The Journal of Neuroscience.

[97]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[98]  R. Butcher,et al.  Small-molecule pheromones that control dauer development in Caenorhabditis elegans. , 2007, Nature chemical biology.

[99]  Aravinthan D. T. Samuel,et al.  Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans , 2007, Journal of Experimental Biology.

[100]  L. Vosshall,et al.  Bilateral olfactory sensory input enhances chemotaxis behavior , 2008, Nature Neuroscience.

[101]  Jongkyeong Chung,et al.  cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila , 2008, Nature.

[102]  R. Butcher,et al.  A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components , 2008, Proceedings of the National Academy of Sciences.

[103]  Greg J. Stephens,et al.  Dimensionality and Dynamics in the Behavior of C. elegans , 2007, PLoS Comput. Biol..

[104]  Zhaoyang Feng,et al.  Light-sensitive neurons and channels mediate phototaxis in C. elegans , 2008, Nature Neuroscience.

[105]  Aravinthan D. T. Samuel,et al.  An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior , 2008, Proceedings of the National Academy of Sciences.

[106]  Aravinthan D. T. Samuel,et al.  Olfactory behavior of swimming C. elegans analyzed by measuring motile responses to temporal variations of odorants. , 2008, Journal of Neurophysiology.

[107]  W. A. Johnson,et al.  Sensory mechanisms controlling the timing of larval developmental and behavioral transitions require the Drosophila DEG/ENaC subunit, Pickpocket1. , 2008, Developmental biology.

[108]  Michael H. Dickinson,et al.  TrackFly: Virtual reality for a behavioral system analysis in free-flying fruit flies , 2008, Journal of Neuroscience Methods.

[109]  Andrew T Sornborger,et al.  Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response , 2008, Nature Neuroscience.

[110]  Daniel Ramot,et al.  Thermotaxis is a Robust Mechanism for Thermoregulation in Caenorhabditis elegans Nematodes , 2008, The Journal of Neuroscience.

[111]  B. Nilius,et al.  TRPs in Our Senses , 2008, Current Biology.

[112]  Koutarou D. Kimura,et al.  Temperature Sensing by an Olfactory Neuron in a Circuit Controlling Behavior of C. elegans , 2008, Science.

[113]  P. Garrity,et al.  Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[114]  Makoto Tominaga,et al.  Drosophila Painless Is a Ca2+-Requiring Channel Activated by Noxious Heat , 2008, The Journal of Neuroscience.

[115]  I. Pe’er,et al.  Caenorhabditis elegans mutant allele identification by whole-genome sequencing , 2008, Nature Methods.

[116]  C. Montell,et al.  Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade , 2008, Nature Neuroscience.

[117]  R. Morimoto,et al.  Regulation of the Cellular Heat Shock Response in Caenorhabditis elegans by Thermosensory Neurons , 2008, Science.

[118]  M. Dickinson,et al.  Visually Mediated Motor Planning in the Escape Response of Drosophila , 2008, Current Biology.

[119]  Stefan R. Pulver,et al.  An internal thermal sensor controlling temperature preference in Drosophila , 2008, Nature.

[120]  Phil S. Hartman,et al.  Repeated temperature fluctuation extends the life span of Caenorhabditis elegans in a daf-16-dependent fashion , 2008, Mechanisms of Ageing and Development.

[121]  Yufeng Shen,et al.  Comparing Platforms for C. elegans Mutant Identification Using High-Throughput Whole-Genome Sequencing , 2008, PloS one.

[122]  Alexander Y Katsov,et al.  Motion Processing Streams in Drosophila Are Behaviorally Specialized , 2008, Neuron.

[123]  Daniel Ramot,et al.  Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans , 2008, Nature Neuroscience.

[124]  A. Simoni,et al.  Temperature Entrainment of Drosophila's Circadian Clock Involves the Gene nocte and Signaling from Peripheral Sensory Tissues to the Brain , 2009, Neuron.

[125]  Mark A. Frye,et al.  Flies Require Bilateral Sensory Input to Track Odor Gradients in Flight , 2009, Current Biology.

[126]  Jeannie Chen,et al.  Enhanced Arrestin Facilitates Recovery and Protects Rods Lacking Rhodopsin Phosphorylation , 2009, Current Biology.

[127]  P. Sternberg,et al.  A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans , 2009, Proceedings of the National Academy of Sciences.

[128]  Z. A. Wahab,et al.  Thermal diffusivity determination of liquid trough thermal diffusion length measurement , 2009 .

[129]  Kazushi Yoshida,et al.  Parallel Use of Two Behavioral Mechanisms for Chemotaxis in Caenorhabditis elegans , 2009, The Journal of Neuroscience.

[130]  R. Butcher,et al.  An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. , 2009, Organic letters.

[131]  S. N. Fry,et al.  Visual control of flight speed in Drosophila melanogaster , 2009, Journal of Experimental Biology.

[132]  A. Mochizuki,et al.  Steepness of thermal gradient is essential to obtain a unified view of thermotaxis in C. elegans. , 2009, Journal of theoretical biology.

[133]  K. Yau,et al.  Phototransduction Motifs and Variations , 2009, Cell.

[134]  M. Welsh,et al.  TRPA channels distinguish gravity sensing from hearing in Johnston's organ , 2009, Proceedings of the National Academy of Sciences.

[135]  Pietro Perona,et al.  High-throughput Ethomics in Large Groups of Drosophila , 2009, Nature Methods.

[136]  R. Huey,et al.  Review: Thermal preference in Drosophila. , 2009, Journal of thermal biology.

[137]  Aravinthan D. T. Samuel,et al.  Navigational Decision Making in Drosophila Thermotaxis , 2010, The Journal of Neuroscience.

[138]  Tao Xu,et al.  C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog , 2010, Nature Neuroscience.

[139]  Cornelia I. Bargmann,et al.  Neuropeptide feedback modifies odor-evoked dynamics in C. elegans olfactory neurons , 2010, Nature Neuroscience.

[140]  A. Hoffmann Physiological climatic limits in Drosophila: patterns and implications , 2010, Journal of Experimental Biology.

[141]  W. Schafer,et al.  Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors , 2010, Nature Neuroscience.

[142]  E. Kodama,et al.  Distinct thermal migration behaviors in response to different thermal gradients in Caenorhabditis elegans , 2010, Genes, brain, and behavior.

[143]  Stefan R. Pulver,et al.  Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception , 2010, Nature.

[144]  C. Montell,et al.  Fine Thermotactic Discrimination between the Optimal and Slightly Cooler Temperatures via a TRPV Channel in Chordotonal Neurons , 2010, The Journal of Neuroscience.