Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

Journal of Experimental Biology

Volumn 216, Issue 5, 2013, Pages 850-858

  Stegeman, Gregory W ^a   De Mesquita, Matthew Bueno ^b   Ryu, William S ^a,b   Cutter, Asher D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Behaviour; Caenorhabditis elegans; Genetic variation; Temperature; Thermotaxis

Indexed keywords

ANIMAL; ARTICLE; CAENORHABDITIS; CAENORHABDITIS ELEGANS; GENETICS; PHENOTYPE; PHYSIOLOGY; QUANTITATIVE TRAIT; SPECIES DIFFERENCE; TEMPERATURE; THERMOREGULATION;

ANIMALS; BODY TEMPERATURE REGULATION; CAENORHABDITIS; CAENORHABDITIS ELEGANS; PHENOTYPE; QUANTITATIVE TRAIT, HERITABLE; SPECIES SPECIFICITY; TEMPERATURE;

EID: 84874182715     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.075408     Document Type: Article

References (44)

1. Anderson, J. L., Albergotti, L., Proulx, S., Peden, C., Huey, R. B. and Phillips, P. C. (2007). Thermal preference of Caenorhabditis elegans: a null model and empirical tests. J. Exp. Biol. 210, 3107-3116.
2. Anderson, J. L., Albergotti, L., Ellebracht, B., Huey, R. B. and Phillips, P. C. (2011). Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans? BMC Evol. Biol. 11, 157.
3. Baird, S. E. (2001). Strain-specific variation in the pattern of caudal papillae in Caenorhabditis briggsae (Nematoda : Rhabditidae); implications for species identification. Nematology 3, 373-376.
4. Baird, S. E., Davidson, C. R. and Bohrer, J. C. (2005). The genetics of ray pattern variation in Caenorhabditis briggsae. BMC Evol. Biol. 5, 3.
5. Bendesky, A. and Bargmann, C. I. (2011). Genetic contributions to behavioural diversity at the gene-environment interface. Nat. Rev. Genet. 12, 809-820.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. Cassata, G., Kagoshima, H., Andachi, Y., Kohara, Y., Dürrenberger, M. B., Hall, D. H. and Bürglin, T. R. (2000). The LIM homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron 25, 587-597.
8. Colosimo, M. E., Brown, A., Mukhopadhyay, S., Gabel, C. V., Lanjuin, A. E., Samuel, A. D. T. and Sengupta, P. (2004). Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr. Biol. 14, 2245-2251.
9. Cutter, A. D. and Choi, J. Y. (2010). Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae. Genome Res. 20, 1103-1111.
10. Cutter, A. D., Félix, M.-A., Barrière, A. and Charlesworth, D. (2006). Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173, 2021-2031.
11. Cutter, A. D., Yan, W., Tsvetkov, N., Sunil, S. and Félix, M.-A. (2010). Molecular population genetics and phenotypic sensitivity to ethanol for a globally diverse sample of the nematode Caenorhabditis briggsae. Mol. Ecol. 19, 798-809.
12. Delattre, M. and Félix, M.-A. (2001). Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr. Biol. 11, 631-643.
13. Dolgin, E. S., Félix, M.-A. and Cutter, A. D. (2008). Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100, 304-315.
14. Fodor, A., Riddle, D. L., Nelson, F. K. and Golden, J. W. (1983). Comparison of a new wild-type Caenorhabditis briggsae with laboratory strains of C. briggsae and C. elegans. Nematologica 29, 203-216.
15. Hedgecock, E. M. and Russell, R. L. (1975). Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 72, 4061-4065.
16. Hillier, L. W., Miller, R. D., Baird, S. E., Chinwalla, A., Fulton, L. A., Koboldt, D. C. and Waterston, R. H. (2007). Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol. 5, e167.
17. Hitcho, P. J. and Thorson, R. E. (1972). Behavior of free-living and plant-parasitic nematodes in a thermal gradient. J. Parasitol. 58, 599.
18. Hodgkin, J. and Doniach, T. (1997). Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146, 149-164.
19. Inada, H., Ito, H., Satterlee, J. S., Sengupta, P., Matsumoto, K. and Mori, I. (2006). Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 172, 2239-2252.
20. Ito, H., Inada, H. and Mori, I. (2006). Quantitative analysis of thermotaxis in the nematode Caenorhabditis elegans. J. Neurosci. Methods 154, 45-52.
21. Jovelin, R. and Cutter, A. D. (2011). MicroRNA sequence variation potentially contributes to within-species functional divergence in the nematode Caenorhabditis briggsae. Genetics 189, 967-976.
22. Jurado, P., Kodama, E., Tanizawa, Y. and Mori, I. (2010). Distinct thermal migration behaviors in response to different thermal gradients in Caenorhabditis elegans. Genes Brain Behav. 9, 120-127.
23. Koboldt, D. C., Staisch, J., Thillainathan, B., Haines, K., Baird, S. E., Chamberlin, H. M., Haag, E. S., Miller, R. D. and Gupta, B. P. (2010). A toolkit for rapid gene mapping in the nematode Caenorhabditis briggsae. BMC Genomics 11, 236.
24. Law, E., Nuttley, W. M. and van der Kooy, D. (2004). Contextual taste cues modulate olfactory learning in C. elegans by an occasion-setting mechanism. Curr. Biol. 14, 1303-1308.
25. Luo, L., Clark, D. A., Biron, D., Mahadevan, L. and Samuel, A. D. T. (2006). Sensorimotor control during isothermal tracking in Caenorhabditis elegans. J. Exp. Biol. 209, 4652-4662.
26. McCue, J. F. and Thorson, R. E. (1964). Behavior of parasitic stages of helminths in a thermal gradient. J. Parasitol. 50, 67-71.
27. McGrath, P. T., Rockman, M. V., Zimmer, M., Jang, H., Macosko, E. Z., Kruglyak, L. and Bargmann, C. I. (2009). Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61, 692-699.
28. McGrath, P. T., Xu, Y., Ailion, M., Garrison, J. L., Butcher, R. A. and Bargmann, C. I. (2011). Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477, 321-325.
29. Mori, I. and Ohshima, Y. (1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344-348.
30. Murray, R. L. and Cutter, A. D. (2011). Experimental evolution of sperm count in protandrous self-fertilizing hermaphrodites. J. Exp. Biol. 214, 1740-1747.
31. Nakazato, K. and Mochizuki, A. (2009). Steepness of thermal gradient is essential to obtain a unified view of thermotaxis in C. elegans. J. Theor. Biol. 260, 56-65.
32. Nigon, V. and Dougherty, E. C. (1949). Reproductive patterns and attempts at reciprocal crossing of Rhabditis elegans Maupas, 1900, and Rhabditis briggsae Dougherty and Nigon, 1949 (Nematoda: Rhabditidae). J. Exp. Zool. 112, 485-503.
33. Ohnishi, N., Kuhara, A., Nakamura, F., Okochi, Y. and Mori, I. (2011). Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO J. 30, 1376-1388.
34. Prasad, A., Croydon-Sugarman, M. J. F., Murray, R. L. and Cutter, A. D. (2011). Temperature-dependent fecundity associates with latitude in Caenorhabditis briggsae. Evolution 65, 52-63.
35. Ramot, D., MacInnis, B. L., Lee, H.-C. and Goodman, M. B. (2008). Thermotaxis is a robust mechanism for thermoregulation in Caenorhabditis elegans nematodes. J. Neurosci. 28, 12546-12557.
36. Rockman, M. V. and Kruglyak, L. (2009). Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet. 5, e1000419.
37. Ross, J. A., Koboldt, D. C., Staisch, J. E., Chamberlin, H. M., Gupta, B. P., Miller, R. D., Baird, S. E. and Haag, E. S. (2011). Caenorhabditis briggsae recombinant inbred line genotypes reveal inter-strain incompatibility and the evolution of recombination. PLoS Genet. 7, e1002174.
38. Ryu, W. S. and Samuel, A. D. T. (2002). Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. J. Neurosci. 22, 5727-5733.
39. Samuel, A. D. T., Silva, R. A. and Murthy, V. N. (2003). Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J. Neurosci. 23, 373-376.
40. Satterlee, J. S., Ryu, W. S. and Sengupta, P. (2004). The CMK-1 CaMKI and the TAX-4 Cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans. Curr. Biol. 14, 62-68.
41. Stiernagle, T. (2006). Maintenance of C. elegans. In WormBook: The Online Review of C. elegans Biology (ed. The C. elegans Research Community), doi/10.1895/wormbook.1.101.1.
42. Tanizawa, Y., Kuhara, A., Inada, H., Kodama, E., Mizuno, T. and Mori, I. (2006). Inositol monophosphatase regulates localization of synaptic components and behavior in the mature nervous system of C. elegans. Genes Dev. 20, 3296-3310.
43. Wasserman, S. M., Beverly, M., Bell, H. W. and Sengupta, P. (2011). Regulation of response properties and operating range of the AFD thermosensory neurons by cGMP signaling. Curr. Biol. 21, 353-362.
44. Zariwala, H. A., Miller, A. C., Faumont, S. and Lockery, S. R. (2003). Step response analysis of thermotaxis in Caenorhabditis elegans. J. Neurosci. 23, 4369-4377.