Distributed effects of biological sex define sex-typical motor behavior in Caenorhabditis elegans

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1579-1591

  Mowrey, William R ^a   Bennett, Jessica R ^a   Portman, Douglas S ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

C. elegans; Locomotion; Motor control; Sex differences

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BIOMECHANICS; BODY SIZE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; FEMALE; GEOMETRY; LOCOMOTION; MALE; MOLECULAR BIOLOGY; MOTOR SYSTEM; MUSCULOSKELETAL FUNCTION; NONHUMAN; OLFACTORY NERVE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SENSORY NERVE CELL; SEX DIFFERENCE; SEX TRANSFORMATION;

C. ELEGANS; LOCOMOTION; MOTOR CONTROL; SEX DIFFERENCES;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOMECHANICAL PHENOMENA; BODY SIZE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHOLINERGIC AGONISTS; FEMALE; LEVAMISOLE; LOCOMOTION; LUMINESCENT PROTEINS; MALE; MODELS, BIOLOGICAL; MOTOR ACTIVITY; MUSCLES; NERVOUS SYSTEM; NEURONS; PHYSICAL STIMULATION; PROPRIOCEPTION; SEX CHARACTERISTICS; SEX DIFFERENTIATION;

EID: 84893052227     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4352-13.2014     Document Type: Article

References (64)

1. Alexander RM (2003) Principles of animal locomotion. Princeton: Princeton UP.
2. Anderson DJ (2012) Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol Psychiatry 71: 1081-1089. CrossRef Medline
3. Ardizzi JP, Epstein HF (1987) Immunochemical localization of myosin heavy chain isoforms and paramyosin in developmentally and structurally diverse muscle cell types of the nematode Caenorhabditis elegans. J Cell Biol 105: 2763-2770. CrossRef Medline
4. Barr MM, Garcia LR (2006) Male mating behavior. In: WormBook (Jorgensen EM, Kaplan JM, eds). http: //www. wormbook. org. CrossRef
5. Berri S, Boyle JH, Tassieri M, Hope IA, Cohen N (2009) Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait. HFSP J 3: 186-193. CrossRef Medline
6. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV (2001) Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 21: 1510-1522. Medline
7. Chalfie M, Sulston J, White J, Southgate E, Thomson J, Brenner S (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5: 956-964.
8. Chiel HJ, Beer RD (1997) The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci 20: 553-557. CrossRef Medline
9. Clyne JD, Miesenböck G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133: 354-363. CrossRef Medline
10. Cohen AH (1992) The role of heterarchical control in the evolution of central pattern generators. Brain Behav Evol 40: 112-124. CrossRef Medline
11. Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17: 8259-8269. Medline
12. Cronin CJ, Mendel JE, Mukhtar S, Kim YM, Stirbl RC, Bruck J, Sternberg PW (2005) An automated system for measuring parameters of nematode sinusoidal movement. BMC Genet 6: 5. CrossRef Medline
13. Desai T, Batani D, Bernardinello A, Poletti G, Orsini F, Ullschmied J, Juha L, Skala J, Kralikova B, Krousky E, Pfeifer M, Kadlec C, Mocek T, Prag A, Renner O, Cotelli F, Lamia CL, Zullini A (2003) X-ray microscopy of living multicellular organisms with the Prague Asterix Iodine Laser System. Laser Part Beams 21: 511-516.
14. de Vries GJ, Södersten P (2009) Sex differences in the brain: the relation between structure and function. Horm Behav 55: 589-596. CrossRef Medline
15. Dresdner RD, Katz DF, Berger SA (1980) The propulsion by largeamplitude waves of uniflagellar microorganisms of finite length. J Fluid Mech 97: 591-621. CrossRef
16. Eastman C, Horvitz HR, Jin Y (1999) Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the Caenorhabditis elegans UNC-30 homeodomain protein. J Neurosci 19: 6225-6234. Medline
17. Emmons SW (2005) Male development. In: WormBook (Meyer BJ, ed). http: //www. wormbook. org. CrossRef
18. Emmons SW (2006) Sexual behavior of the Caenorhabditis elegans male. Int Rev Neurobiol 69: 99-123. Medline
19. Fang-Yen C, Wyart M, Xie J, Kawai R, Kodger T, Chen S, Wen Q, Samuel AD (2010) Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 107: 20323-20328. CrossRef Medline
20. Field EF, Whishaw IQ (2008) Sex differences in the organization of movement. In: Sex differences in the brain: from genes to behavior (Becker JB, Berkley KJ, Geary N, Hampson E, Herman JP, eds), pp 155-175. New York: Oxford UP.
21. Fitch DH (2000) Evolution of "rhabditidae" and the male tail. J Nematol 32: 235-244. Medline
22. Gray J, Hancock GJ (1955) The propulsion of sea-urchin spermatozoa. J Exp Biol 32: 802-814.
23. Gray J, Lissmann HW (1964) The locomotion of nematodes. J Exp Biol 41: 135-154. Medline
24. Haycraft CJ, Swoboda P, Taulman PD, Thomas JH, Yoder BK (2001) The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128: 1493-1505. Medline
25. Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4: 136-138. CrossRef Medline
26. Hodgkin J (1987) A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1: 731-745. CrossRef Medline
27. Hodgkin JA (1974) Genetic and anatomical aspects of the Caenorhabditis elegans male. PhD thesis, University of Cambridge.
28. Hunter CP, Wood WB (1990) The tra-1 gene determines sexual phenotype cell-autonomously in C. elegans. Cell 63: 1193-1204. CrossRef Medline
29. Kelly CD, Bussière LF, Gwynne DT (2008) Sexual selection for male mobility in a giant insect with female-biased size dimorphism. AmNat 172: 417-423. CrossRef Medline
30. Komatsu H, Mori I, Rhee JS, Akaike N, Ohshima Y (1996) Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17: 707-718. CrossRef Medline
31. Lee K, Portman DS (2007) Neural sex modifies the function of a C. elegans sensory circuit. Curr Biol 17: 1858-1863. CrossRef Medline
32. Li W, Feng Z, Sternberg P, Xu X (2006) A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440: 684-687. CrossRef Medline
33. Lighthill J (1976) Flagellar hydrodynamics. SIAM Rev 18: 161-230. CrossRef
34. Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW (2004) Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J Neurosci 24: 7427-7434. CrossRef Medline
35. Loer CM, Kenyon CJ (1993) Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13: 5407-5417. Medline
36. Lum DH, Kuwabara PE, Zarkower D, Spence AM (2000) Direct proteinprotein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans. Genes Dev 14: 3153-3165. Medline
37. McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, Kruglyak L, Bargmann CI (2009) Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61: 692-699. CrossRef Medline
38. Mehra A, Gaudet J, Heck L, Kuwabara PE, Spence AM (1999) Negative regulation of male development in Caenorhabditis elegans by a proteinprotein interaction between TRA-2A and FEM-3. Genes Dev 13: 1453-1463. CrossRef Medline
39. Mello CC, Fire A (1995) DNA transformation. In: Caenorhabditis elegans: modern biological analysis of an organism (Epstein HF, Shakes DC, eds). San Diego: Academic.
40. Mowrey WR, Portman DS (2012) Sex differences in behavioral decisionmaking and the modulation of shared neural circuits. Biol Sex Differ 3: 8. CrossRef Medline
41. Nass R, Hall DH, Miller DM 3rd, Blakely RD (2002) Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci U S A 99: 3264-3269. CrossRef Medline
42. Nishikawa K, Biewener AA, Aerts P, Ahn AN, Chiel HJ, Daley MA, Daniel TL, Full RJ, Hale ME, Hedrick TL, Lappin AK, Nichols TR, Quinn RD, Satterlie RA, Szymik B (2007) Neuromechanics: an integrative approach for understanding motor control. Integr Comp Biol 47: 16-54. CrossRef Medline
43. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, Horvitz HR, Jorgensen EM, Meyer BJ (1997) Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J Neurosci 17: 8061-8073. Medline
44. Park SJ, Goodman MB, Pruitt BL (2007) Analysis of nematode mechanics by piezoresistive displacement clamp. Proc Natl Acad Sci U S A 104: 17376-17381. CrossRef Medline
45. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487. CrossRef Medline
46. Portman DS (2007) Genetic control of sex differences in C. elegans neurobiology and behavior. Adv Genet 59: 1-37. CrossRef Medline
47. Poulin R (1997) Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes. Biol J Linn Soc 62: 567-580. CrossRef
48. Rand JB (2007) Acetylcholine. In: WormBook (Joregensen EM, Kaplan JM, eds) http: //www. wormbook. org. CrossRef
49. Reeve JP, Fairbairn DJ (1999) Change in sexual size dimorphism as a correlated response to selection on fecundity. Heredity 83: 697-706. CrossRef Medline
50. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26: 619-631. CrossRef Medline
51. Schafer WF (2006) Genetics of egg-laying in worms. Annu Rev Genet 40: 487-509. CrossRef Medline
52. Schindelman G, Whittaker AJ, Thum JY, Gharib S, Sternberg PW (2006) Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord. BMC Biol 4: 26. CrossRef Medline
53. Sternberg P (2005) Vulval development. In: WormBook (Meyer BJ, ed) http: //www. wormbook. org. CrossRef
54. Sulston JE, Horvitz HR (1977) Postembryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56: 110-156. CrossRef Medline
55. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564. CrossRef Medline
56. Tirtaatmadja V, Dunstan DE, Boger DV (2001) Rheology of dextran solutions. J Non-Newtonian Fluid Mech 97: 295-301. CrossRef
57. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207-218. CrossRef Medline
58. Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, de Bono M (2010) Whole genome sequencing highlights genetic changes associated with laboratory domestication of C. elegans. PLOS One 5: e13922. CrossRef Medline
59. Wen Q, Po MD, Hulme E, Chen S, Liu X, Kwok SW, Gershow M, Leifer AM, Butler V, Fang-Yen C, Kawano T, Schafer WR, Whitesides G, Wyart M, Chklovskii DB, Zhen M, Samuel AD (2012) Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion. Neuron 76: 750-761. CrossRef Medline
60. White JG (1988) The anatomy. In: The nematode Caenorhabditis elegans (Wood WB, ed). Woodbury, NY: Cold Spring Harbor Laboratory.
61. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314: 1-340. CrossRef
62. White JQ, Nicholas TJ, Gritton J, Truong L, Davidson ER, Jorgensen EM (2007) The sensory circuitry for sexual attraction in C. elegans males. Curr Biol 17: 1847-1857. CrossRef Medline
63. Winnier AR, Meir JY, Ross JM, Tavernarakis N, Driscoll M, Ishihara T, Katsura I, MillerDM3rd (1999) UNC-4/UNC-37-dependent repression of motor neuron-specific genes controls synaptic choice in Caenorhabditis elegans. Genes Dev 13: 2774-2786. CrossRef Medline
64. Wolff JR, Zarkower D (2008) Somatic sexual differentiation in Caenorhabditis elegans. Curr Top Dev Biol 83: 1-39. CrossRef Medline