1932

Abstract

The recently determined connectome of the adult male, together with the known connectome of the hermaphrodite, opens up the possibility for a comprehensive description of sexual dimorphism in this species and the identification and study of the neural circuits underlying sexual behaviors. The nervous system consists of 294 neurons shared by both sexes plus neurons unique to each sex, 8 in the hermaphrodite and 91 in the male. The sex-specific neurons are well integrated within the remainder of the nervous system; in the male, 16% of the input to the shared component comes from male-specific neurons. Although sex-specific neurons are involved primarily, but not exclusively, in controlling sex-unique behavior—egg-laying in the hermaphrodite and copulation in the male—these neurons act together with shared neurons to make navigational choices that optimize reproductive success. Sex differences in general behaviors are underlain by considerable dimorphism within the shared component of the nervous system itself, including dimorphism in synaptic connectivity.

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2018-07-08
2024-03-29
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Literature Cited

  1. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR 2005. Tyramine functions independently of octopamine in the Caenorhabditiselegans nervous system. Neuron 46:247–60
    [Google Scholar]
  2. Antebi A, Culotti JG, Hedgecock EM 1998. daf-12 regulates developmental age and the dauer alternative in Caenorhabditiselegans. Development 125:1191–205
    [Google Scholar]
  3. Baird SE, Fitch DH, Kassem IA, Emmons SW 1991. Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C.elegans male tail. Development 113:515–26
    [Google Scholar]
  4. Banerjee N, Bhattacharya R, Gorczyca M, Collins KM, Francis MM 2017. Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C.elegans egg-laying behavior. PLOS Genet 13:e1006697
    [Google Scholar]
  5. Barr MM, Garcia LR 2006. Male mating behavior. WormBook: The Online Review of C. elegans Biology [online] The C.elegans Research Community. http://www.wormbook.org/chapters/www_malematingbehavior/malematingbehavior.html
    [Google Scholar]
  6. Barr MM, Garcia R, Portman DS 2018. Sexual dimorphism and sex differences in C.elegans neuronal development and behavior. Genetics 208:909–35
    [Google Scholar]
  7. Barr MM, Sternberg PW 1999. A polycystic kidney-disease gene homologue required for male mating behaviour in C.elegans. Nature 401:386–89
    [Google Scholar]
  8. Barrios A 2014. Exploratory decisions of the Caenorhabditiselegans male: a conflict of two drives. Semin. Cell Dev. Biol. 33:10–17
    [Google Scholar]
  9. Barrios A, Ghosh R, Fang C, Emmons SW, Barr MM 2012. PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C.elegans. Nat. Neurosci 15:1675–82
    [Google Scholar]
  10. Barrios A, Nurrish S, Emmons SW 2008. Sensory regulation of C.elegans male mate-searching behavior. Curr. Biol. 18:1865–71
    [Google Scholar]
  11. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S 1985. The neural circuit for touch sensitivity in Caenorhabditiselegans. J. Neurosci 5:956–64
    [Google Scholar]
  12. Collins KM, Bode A, Fernandez RW, Tanis JE, Brewer JC et al. 2016. Activity of the C.elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition. eLife 5:e21126
    [Google Scholar]
  13. Correa PA, Gruninger T, García LR 2015. DOP-2 D2-like receptor regulates UNC-7 innexins to attenuate recurrent sensory motor neurons during C.elegans copulation. J. Neurosci. 35:9990–10004
    [Google Scholar]
  14. Correa P, LeBoeuf B, García LR 2012. C.elegans dopaminergic D2-like receptors delimit recurrent cholinergic-mediated motor programs during a goal-oriented behavior. PLOS Genet 8:e1003015
    [Google Scholar]
  15. Desai C, Garriga G, McIntire SL, Horvitz HR 1988. A genetic pathway for the development of the Caenorhabditiselegans HSN motor neurons. Nature 336:638–46
    [Google Scholar]
  16. Desai C, Horvitz HR 1989. Caenorhabditiselegans mutants defective in the functioning of the motor neurons responsible for egg laying. Genetics 121:703–21
    [Google Scholar]
  17. Emmons SW 2016. Connectomics, the final frontier. Curr. Top. Dev. Biol. 116:315–30
    [Google Scholar]
  18. Fagan KA, Luo J, Lagoy RC, Schroeder FC, Albrecht DR, Portman DS 2018. A chemosensory switch couples genetic sex to behavioral valence. Curr. Biol. 28:902–14.e5
    [Google Scholar]
  19. Fenk LA, de Bono M 2015. Environmental CO2 inhibits Caenorhabditiselegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity. PNAS 112:E3525–34
    [Google Scholar]
  20. García LR 2014. Regulation of sensory motor circuits used in C.elegans male intromission behavior. Semin. Cell Dev. Biol. 33:42–49
    [Google Scholar]
  21. Garcia LR, LeBoeuf B, Koo P 2007. Diversity in mating behavior of hermaphrodite and male-female Caenorhabditis nematodes. Genetics 175:1761–71
    [Google Scholar]
  22. Garcia LR, Mehta P, Sternberg PW 2001. Regulation of distinct muscle behaviors controls the C.elegans male's copulatory spicules during mating. Cell 107:777–88
    [Google Scholar]
  23. García LR, Portman DS 2016. Neural circuits for sexually dimorphic and sexually divergent behaviors in Caenorhabditiselegans.Curr.Opin. Neurobiol 38:46–52
    [Google Scholar]
  24. Garcia LR, Sternberg PW 2003. Caenorhabditiselegans UNC-103 ERG-like potassium channel regulates contractile behaviors of sex muscles in males before and during mating. J. Neurosci. 23:2696–705
    [Google Scholar]
  25. Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, Bargmann CI 2012. Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science 338:540–43
    [Google Scholar]
  26. Gravato-Nobre MJ, Stroud D, O'Rourke D, Darby C, Hodgkin J 2011. Glycosylation genes expressed in seam cells determine complex surface properties and bacterial adhesion to the cuticle of Caenorhabditiselegans. Genetics 187:141–55
    [Google Scholar]
  27. Gray JM, Hill JJ, Bargmann CI 2005. A circuit for navigation in Caenorhabditiselegans. PNAS 102:3184–91
    [Google Scholar]
  28. Gruninger TR, Gualberto DG, LeBoeuf B, Garcia LR 2006. Integration of male mating and feeding behaviors in Caenorhabditiselegans. J. Neurosci 26:169–79
    [Google Scholar]
  29. Hallem EA, Spencer WC, McWhirter RD, Zeller G, Henz SR et al. 2011. Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditiselegans. PNAS 108:254–59
    [Google Scholar]
  30. Hardaker LA, Singer E, Kerr R, Zhao B, Schafer WR 2001. Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditiselegans. J. Neurobiol 49:303–13
    [Google Scholar]
  31. Hart MP, Hobert O 2018. Neurexin controls plasticity of a mature, sexually dimorphic neuron. Nature 553:165–70
    [Google Scholar]
  32. Hilbert ZA, Kim DH 2017. Sexually dimorphic control of gene expression in sensory neurons regulates decision-making behavior in C. elegans. eLife 6:e21166
    [Google Scholar]
  33. Izrayelit Y, Srinivasan J, Campbell SL, Jo Y, von Reuss SH et al. 2012. Targeted metabolomics reveals a male pheromone and sex-specific ascaroside biosynthesis in Caenorhabditiselegans. ACS Chem. Biol 7:1321–25
    [Google Scholar]
  34. Jarrell TA, Wang Y, Bloniarz AE, Brittin CA, Xu M et al. 2012. The connectome of a decision-making neural network. Science 337:437–44
    [Google Scholar]
  35. Jee C, Goncalves JF, LeBoeuf B, Garcia LR 2016. CRF-like receptor SEB-3 in sex-common interneurons potentiates stress handling and reproductive drive in C.elegans. Nat. Commun 7:11957
    [Google Scholar]
  36. Kleemann G, Jia L, Emmons SW 2008. Regulation of Caenorhabditiselegans male mate searching behavior by the nuclear receptor DAF-12. Genetics 180:2111–22
    [Google Scholar]
  37. Kleemann GA, Basolo AL 2007. Facultative decrease in mating resistance in hermaphroditic Caenorhabditiselegans with self-sperm depletion. Anim. Behav. 74:1339–47
    [Google Scholar]
  38. Klein M, Krivov SV, Ferrer AJ, Luo L, Samuel ADT, Karplus M 2017. Exploratory search during directed navigation in C.elegans and Drosophila larva. eLife 6:e30503
    [Google Scholar]
  39. Koo PK, Bian X, Sherlekar AL, Bunkers MR, Lints R 2011. The robustness of Caenorhabditiselegans male mating behavior depends on the distributed properties of ray sensory neurons and their output through core and male-specific targets. J. Neurosci. 31:7497–510
    [Google Scholar]
  40. LeBoeuf B, Correa P, Jee C, García LR 2014. Caenorhabditiselegans male sensory-motor neurons and dopaminergic support cells couple ejaculation and post-ejaculatory behaviors. eLife 3:e02938
    [Google Scholar]
  41. LeBoeuf B, Garcia LR 2012. Cell excitability necessary for male mating behavior in Caenorhabditiselegans is coordinated by interactions between Big Current and Ether-A-Go-Go family K+ channels. Genetics 190:1025–41
    [Google Scholar]
  42. LeBoeuf B, Garcia LR 2017. Caenorhabditiselegans male copulation circuitry incorporates sex-shared defecation components to promote intromission and sperm transfer. G3 7:647–62
    [Google Scholar]
  43. Lee K, Portman DS 2007. Neural sex modifies the function of a C.elegans sensory circuit. Curr. Biol. 17:1858–63
    [Google Scholar]
  44. Leicht EA, Newman MEJ 2008. Community structure in directed networks. Phys. Rev. Lett. 100:118703–8
    [Google Scholar]
  45. Leighton DHW, Choe A, Wu SY, Sternberg PW 2014. Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditiselegans. PNAS 111:17905–10
    [Google Scholar]
  46. Leighton DHW, Sternberg PW 2016. Mating pheromones of Nematoda: olfactory signaling with physiological consequences. Curr. Opin. Neurobiol. 38:119–24
    [Google Scholar]
  47. Li W, Feng Z, Sternberg PW, Xu XZ 2006. A C.elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684–87
    [Google Scholar]
  48. Lints R, Emmons SW 1999. Patterning of dopaminergic neurotransmitter identity among Caenorhabditiselegans ray sensory neurons by a TGFβ family signaling pathway and a Hox gene. Development 126:5819–31
    [Google Scholar]
  49. Lints R, Jia L, Kim K, Li C, Emmons SW 2004. Axial patterning of C.elegans male sensilla identities by selector genes. Dev. Biol. 269:137–51
    [Google Scholar]
  50. Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW 2004. Mate searching in Caenorhabditiselegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 24:7427–34
    [Google Scholar]
  51. Liu KS, Sternberg PW 1995. Sensory regulation of male mating behavior in Caenorhabditiselegans. Neuron 14:79–89
    [Google Scholar]
  52. Liu Y, LeBoeuf B, Garcia LR 2007. q-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditiselegans mating behavior. J. Neurosci. 27:1411–21
    [Google Scholar]
  53. Liu Y, LeBeouf B, Guo X, Correa PA, Gualberto DG et al. 2011. A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditiselegans male copulation. PLOS Genet 7:e1001326
    [Google Scholar]
  54. Meisel JD, Panda O, Mahanti P, Schroeder FC, Kim DH 2014. Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C.elegans. Cell 159:267–80
    [Google Scholar]
  55. Morsci NS, Haas LA, Barr MM 2011. Sperm status regulates sexual attraction in Caenorhabditiselegans. Genetics 189:1341–46
    [Google Scholar]
  56. Mowrey WR, Bennett JR, Portman DS 2014. Distributed effects of biological sex define sex-typical motor behavior in Caenorhabditiselegans. J.Neurosci. Res 34:1579–91
    [Google Scholar]
  57. Narayan A, Venkatachalam V, Durak O, Reilly DK, Bose N et al. 2016. Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditiselegans. PNAS 113:E1392–401
    [Google Scholar]
  58. Newman MEJ 2006. Modularity and community structure in networks. PNAS 103:8577–82
    [Google Scholar]
  59. Oren-Suissa M, Bayer EA, Hobert O 2016. Sex-specific pruning of neuronal synapses in Caenorhabditiselegans. Nature 533:206–11
    [Google Scholar]
  60. Pierce-Shimomura JT, Morse TM, Lockery SR 1999. The fundamental role of pirouettes in Caenorhabditiselegans chemotaxis. J. Neurosci. 19:9557–69
    [Google Scholar]
  61. Portman DS 2017. Sexual modulation of sex‐shared neurons and circuits in Caenorhabditiselegans. J.Neurosci. Res 95:527–38
    [Google Scholar]
  62. Pungaliya C, Srinivasan J, Fox BW, Malik RU, Ludewig AH et al. 2009. A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditiselegans. PNAS 106:7708–13
    [Google Scholar]
  63. Ringstad N, Horvitz HR 2008. FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C.elegans. Nat. Neurosci 11:1168–76
    [Google Scholar]
  64. Roberts WM, Augustine SB, Lawton KJ, Lindsay TH, Thiele TR et al. 2016. A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans. eLife 5:e12572
    [Google Scholar]
  65. Ryan DA, Miller RM, Lee K, Neal SJ, Fagan KA et al. 2014. Sex, age, and hunger regulate behavioral prioritization through dynamic modulation of chemoreceptor expression. Curr. Biol. 24:2509–17
    [Google Scholar]
  66. Sakai N, Iwata R, Yokoi S, Butcher RA, Clardy J et al. 2013. A sexually conditioned switch of chemosensory behavior in C.elegans. PLOS ONE 8:e68676
    [Google Scholar]
  67. Sammut M, Cook SJ, Nguyen KCQ, Felton T, Hall DH et al. 2015. Glia-derived neurons are required for sex-specific learning in C.elegans. Nature 526:385–90
    [Google Scholar]
  68. Serrano-Saiz E, Oren-Suissa M, Bayer EA, Hobert O 2017a. Sexually dimorphic differentiation of a C.elegans hub neuron is cell autonomously controlled by a conserved transcription factor. Curr. Biol. 27:199–209
    [Google Scholar]
  69. Serrano-Saiz E, Pereira L, Gendrel M, Aghayeva U, Battacharya A et al. 2017b. A neurotransmitter atlas of the Caenorhabditiselegans male nervous system reveals sexually dimorphic neurotransmitter usage. Genetics 206:1251–69
    [Google Scholar]
  70. Schafer WR 2005. Egg-laying. WormBook: The Online Review of C. elegans Biology [online] The C.elegans Research Community. http://www.wormbook.org/chapters/www_egglaying/egglaying.html
    [Google Scholar]
  71. Schindelman G, Whittaker AJ, Thum JY, Gharib S, Sternberg PW 2006. Initiation of male sperm-transfer behavior in Caenorhabditiselegans requires input from the ventral nerve cord. BMC Biol 4:26
    [Google Scholar]
  72. Sherlekar AL, Janssen A, Siehr MS, Koo PK, Caflisch L et al. 2013. The C.elegans male exercises directional control during mating through cholinergic regulation of sex-shared command interneurons. PLOS ONE 8:e60597
    [Google Scholar]
  73. Sherlekar AL, Lints R 2014. Nematode tango milonguero—the C.elegans male's search for the hermaphrodite vulva. Semin. Cell Dev. Biol. 33:34–41
    [Google Scholar]
  74. Simon JM, Sternberg PW 2002. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditiselegans. PNAS 99:1598–603
    [Google Scholar]
  75. Srinivasan J, Kaplan J, Kaplan F, Ajredini R, Zhacharia C et al. 2008. A blend of small molecules regulates both mating and development in Caenorhabditiselegans. Nature 454:1115–18
    [Google Scholar]
  76. Srinivasan J, von Reuss SH, Bose N, Zaslaver A, Mahanti P et al. 2012. A modular library of small molecule signals regulates social behaviors in Caenorhabditiselegans. PLOS Biol 10:e1001237
    [Google Scholar]
  77. Stephens GJ, Bueno de Mesquita M, Ryu WS, Bialek W 2011. Emergence of long timescales and stereotyped behaviors in Caenorhabditiselegans. PNAS 108:7286–89
    [Google Scholar]
  78. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS 2008. Dimensionality and dynamics in the behavior of C.elegans. PLOSComput. Biol 4:e1000028
    [Google Scholar]
  79. Stephens GJ, Johnson-Kerner B, Bialek W, Ryu WS 2010. From modes to movement in the behavior of Caenorhabditiselegans. PLOS ONE 5:e13914
    [Google Scholar]
  80. Sulston JE, Albertson DG, Thomson JN 1980. The Caenorhabditiselegans male: postembryonic development of nongonadal structures. Dev. Biol. 78:542–76
    [Google Scholar]
  81. Trent C, Tsung N, Horvitz HR 1983. Egg-laying defective mutants of the nematode Caenorhabditiselegans. Genetics 104:619–47
    [Google Scholar]
  82. Waggoner LE, Zhou GT, Schafer RW, Schafer WR 1998. Control of alternative behavioral states by serotonin in Caenorhabditiselegans. Neuron 21:203–14
    [Google Scholar]
  83. White JG, Southgate E, Thomson JN, Brenner S 1986. The structure of the nervous system of the nematode Caenorhabditiselegans. Philos. Trans. R. Soc. B 314:1–340
    [Google Scholar]
  84. White JQ, Jorgensen EM 2012. Sensation in a single neuron pair represses male behavior in hermaphrodites. Neuron 75:593–600
    [Google Scholar]
  85. 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. 17:1847–57
    [Google Scholar]
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