Acoustic duetting in Drosophila virilis relies on the integration of auditory and tactile signals

eLife

Volumn 4, Issue JUNE, 2015, Pages 1-23

  LaRue, Kelly M ^a   Clemens, Jan ^a   Berman, Gordon J ^a   Murthy, Mala ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; AUDITORY DISCRIMINATION; DROSOPHILA VIRILIS; FEMALE; GENITAL SYSTEM; HEARING; MALE; MATING; NONHUMAN; PREDICTION; PULSE RATE; RESPONSE TIME; SENSORY STIMULATION; SEX DIFFERENCE; VIDEORECORDING; ANIMAL; ANIMAL MODEL; AUDITORY STIMULATION; BIOLOGICAL MODEL; COURTSHIP; DROSOPHILA; PHYSIOLOGY; SOUND DETECTION; TOUCH; VOCALIZATION;

ANIMALIA; DROSOPHILA VIRILIS; HEXAPODA;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; COURTSHIP; CUES; DROSOPHILA; FEMALE; MALE; MODELS, ANIMAL; MODELS, BIOLOGICAL; SOUND SPECTROGRAPHY; TOUCH PERCEPTION; VIDEO RECORDING; VOCALIZATION, ANIMAL;

EID: 84933038070     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07277     Document Type: Article

References (67)

1. Arthur BJ, Sunayama-Morita T, Coen P, Murthy M, Stern DL. 2013. Multi-channel acoustic recording and automated analysis of Drosophila courtship songs. BMC Biology 11:11. doi: 10.1186/1741-7007-11-11.
2. Aspi J, Hoikkala A. 1993. Laboratory and natural heritabilities of male courtship song characters in Drosophila montana and D. littoralis. Heredity 70:400-406. doi: 10.1038/hdy.1993.56.
3. Bailey WJ. 2003. Insect duets: underlying mechanisms and their evolution. Physiological Entomology 28:157-174. doi: 10.1046/j.1365-3032.2003.00337.x.
4. Bailey WJ, Hammond TJ. 2003. Duetting in insects-does call length influence reply latency? Journal of Zoology 260:267-274. doi: 10.1017/S0952836903003728.
5. Bassett AR, Liu JL. 2014. CRISPR/Cas9 and genome editing in Drosophila. Journal of Genetics and Genomics 41: 7-19. doi: 10.1016/j.jgg.2013.12.004.
6. Benton R. 2007. Sensitivity and specificity in Drosophila pheromone perception. Trends in Neurosciences 30: 512-519. doi: 10.1016/j.tins.2007.07.004.
7. Clutton-Brock T. 2007. Sexual selection in males and females. Science 318:1882-1885. doi: 10.1126/science. 1133311.
8. Clyne JD, Miesenbock G. 2008. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133:354-363. doi: 10.1016/j.cell.2008.01.050.
9. Coen P, Clemens J, Weinstein AJ, Pacheco DA, Deng Y, Murthy M. 2014. Dynamic sensory cues shape song structure in Drosophila. Nature 507:233-237. doi: 10.1038/nature13131.
10. Demir E, Dickson BJ. 2005. Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121:785-794. doi: 10.1016/j.cell.2005.04.027.
11. Dickson BJ. 2008. Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904-909. doi: 10. 1126/science.1159276.
12. Donegan J, Ewing AW. 1980. Duetting in Drosophila and Zaprionus species. Animal Behaviour 28:1289. doi: 10. 1016/S0003-3472(80)80119-9.
13. Drosophila 12 Genomes Consortium, Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, Pollard DA, Sackton TB, Larracuente AM, Singh ND, Abad JP, Abt DN, Adryan B, Aguade M, Akashi H, Anderson WW, Aquadro CF, Ardell DH, Arguello R, Artieri CG, Barbash DA, Barker D, Barsanti P, Batterham P, Batzoglou S, Begun D, Bhutkar A, Blanco E, Bosak SA, Bradley RK, Brand AD, Brent MR, Brooks AN, Brown RH, Butlin RK, Caggese C, Calvi BR, Bernardo de Carvalho A, Caspi A, Castrezana S, Celniker SE, Chang JL, Chapple C, Chatterji S, Chinwalla A, Civetta A, Clifton SW, Comeron JM, Costello JC, Coyne JA, Daub J, David RG, Delcher AL, Delehaunty K, Do CB, Ebling H, Edwards K, Eickbush T, Evans JD, Filipski A, Findeiss S, Freyhult E, Fulton L, Fulton R, Garcia AC, Gardiner A, Garfield DA, Garvin BE, Gibson G, Gilbert D, Gnerre S, Godfrey J, Good R, Gotea V, Gravely B, Greenberg AJ, Griffiths-Jones S, Gross S, Guigo R, Gustafson EA, Haerty W, Hahn MW, Halligan DL, Halpern AL, Halter GM, Han MV, Heger A, Hillier L, Hinrichs AS, Holmes I, Hoskins RA, Hubisz MJ, Hultmark D, Huntley MA, Jaffe DB, Jagadeeshan S, Jeck WR, Johnson J, Jones CD, Jordan WC, Karpen GH, Kataoka E, Keightley PD, Kheradpour P, Kirkness EF, Koerich LB, Kristiansen K, Kudrna D, Kulathinal RJ, Kumar S, Kwok R, Lander E, Langley CH, Lapoint R, Lazzaro BP, Lee SJ, Levesque L, Li R, Lin CF, Lin MF, Lindblad-Toh K, Llopart A, Long M, Low L, Lozovsky E, Lu J, Luo M, Machado CA, Makalowski W, Marzo M, Matsuda M, Matzkin L, McAllister B, McBride CS, McKernan B, McKernan K, Mendez-Lago M, Minx P, Mollenhauer MU, Montooth K, Mount SM, Mu X, Myers E, Negre B, Newfeld S, Nielsen R, Noor MA, O'Grady P, Pachter L, Papaceit M, Parisi MJ, Parisi M, Parts L, Pedersen JS, Pesole G, Phillippy AM, Ponting CP, Pop M, Porcelli D, Powell JR, Prohaska S, Pruitt K, Puig M, Quesneville H, Ram KR, Rand D, Rasmussen MD, Reed LK, Reenan R, Reily A, Remington KA, Rieger TT, Ritchie MG, Robin C, Rogers YH, Rohde C, Rozas J, Rubenfield MJ, Ruiz A, Russo S, Salzberg SL, Sanchez-Gracia A, Saranga DJ, Sato H, Schaeffer SW, Schatz MC, Schlenke T, Schwartz R, Segarra C, Singh RS, Sirot L, Sirota M, Sisneros NB, Smith CD, Smith TF, Spieth J, Stage DE, Stark A, Stephan W, Strausberg RL, Strempel S, Sturgill D, Sutton G, Sutton GG, Tao W, Teichmann S, Tobari YN, Tomimura Y, Tsolas JM, Valente VL, Venter E, Venter JC, Vicario S, Vieira FG, Vilella AJ, Villasante A, Walenz B, Wang J, Wasserman M, Watts T, Wilson D, Wilson RK, Wing RA, Wolfner MF, Wong A, Wong GK, Wu CI, Wu G, Yamamoto D, Yang HP, Yang SP, Yorke JA, Yoshida K, Zdobnov E, Zhang P, Zhang Y, Zimin AV, Baldwin J, Abdouelleil A, Abdulkadir J, Abebe A, Abera B, Abreu J, Acer SC, Aftuck L, Alexander A, An P, Anderson E, Anderson S, Arachi H, Azer M, Bachantsang P, Barry A, Bayul T, Berlin A, Bessette D, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Bourzgui I, Brown A, Cahill P, Channer S, Cheshatsang Y, Chuda L, Citroen M, Collymore A, Cooke P, Costello M, D'Aco K, Daza R, De Haan G, DeGray S, DeMaso C, Dhargay N, Dooley K, Dooley E, Doricent M, Dorje P, Dorjee K, Dupes A, Elong R, Falk J, Farina A, Faro S, Ferguson D, Fisher S, Foley CD, Franke A, Friedrich D, Gadbois L, Gearin G, Gearin CR, Giannoukos G, Goode T, Graham J, Grandbois E, Grewal S, Gyaltsen K, Hafez N, Hagos B, Hall J, Henson C, Hollinger A, Honan T, Huard MD, Hughes L, Hurhula B, Husby ME, Kamat A, Kanga B, Kashin S, Khazanovich D, Kisner P, Lance K, Lara M, Lee W, Lennon N, Letendre F, LeVine R, Lipovsky A, Liu X, Liu J, Liu S, Lokyitsang T, Lokyitsang Y, Lubonja R, Lui A, MacDonald P, Magnisalis V, Maru K, Matthews C, McCusker W, McDonough S, Mehta T, Meldrim J, Meneus L, Mihai O, Mihalev A, Mihova T, Mittelman R, Mlenga V, Montmayeur A, Mulrain L, Navidi A, Naylor J, Negash T, Nguyen T, Nguyen N, Nicol R, Norbu C, Norbu N, Novod N, O'Neill B, Osman S, Markiewicz E, Oyono OL, Patti C, Phunkhang P, Pierre F, Priest M, Raghuraman S, Rege F, Reyes R, Rise C, Rogov P, Ross K, Ryan E, Settipalli S, Shea T, Sherpa N, Shi L, Shih D, Sparrow T, Spaulding J, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Strader C, Tesfaye S, Thomson T, Thoulutsang Y, Thoulutsang D, Topham K, Topping I, Tsamla T, Vassiliev H, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Young G, Yu Q, Zembek L, Zhong D, Zimmer A, Zwirko Z, Jaffe DB, Alvarez P, BrockmanW, Butler J, Chin C, Gnerre S, Grabherr M, Kleber M, Mauceli E, MacCallum I. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203-218. doi: 10.1038/nature06341.
14. Elliott MT, Wing AM, Welchman AE. 2010. Multisensory cues improve sensorimotor synchronisation. The European Journal of Neuroscience 31:1828-1835. doi: 10.1111/j.1460-9568.2010.07205.x.
15. Ewing AW, Bennet-Clark HC. 1968. The courtship songs of Drosophila. Behaviour 31:288-301. doi: 10.1163/ 156853968X00298.
16. Fabre CC, Casal J, Lawrence PA. 2008. The abdomen of Drosophila: does planar cell polarity orient the neurons of mechanosensory bristles? Neural Development 3:12. doi: 10.1186/1749-8104-3-12.
17. Fan P, Manoli DS, Ahmed OM, Chen Y, Agarwal N, Kwong S, Cai AG, Neitz J, Renslo A, Baker BS, Shah NM. 2013. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154:89-102. doi: 10. 1016/j.cell.2013.06.008.
18. Fetsch CR, Pouget A, DeAngelis GC, Angelaki DE. 2012. Neural correlates of reliability-based cue weighting during multisensory integration. Nature Neuroscience 15:146-154. doi: 10.1038/nn.2983.
19. Fortune ES, Rodríguez C, Li D, Ball GF, Coleman MJ. 2011. Neural mechanisms for the coordination of duet singing in wrens. Science 334:666-670. doi: 10.1126/science.1209867.
20. Gick B, Derrick D. 2009. Aero-tactile integration in speech perception. Nature 462:502-504. doi: 10.1038/ nature08572.
21. Gopfert MC, Robert D. 2002. The mechanical basis of Drosophila audition. The Journal of Experimental Biology 205:1199-1208.
22. Haimoff EH. 1986. Convergence in the duetting of monogamous Old World primates. Journal of Human Evolution 15:51-59. doi: 10.1016/S0047-2484(86)80065-3.
23. Hall ML. 2004. A review of hypotheses for the functions of avian duetting. Behavioral Ecology and Sociobiology 55: 415-430. doi: 10.1007/s00265-003-0741-x.
24. Hall ML. 2009. Vocal duetting in birds. Advanced in the Study of Behavior 40:67-121.
25. Heller KG, von Helversen D. 1986. Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response and matching male sensory time window. Behavioural Ecology and Sociobiology 18:189-198. doi: 10.1007/BF00290822.
26. Huttunen S, Aspi J, Schlötterer C, Routtu J, Hoikkala A. 2008. Variation in male courtship song traits in Drosophila virilis: the effects of selection and drift on song divergence at the intraspecific level. Behavior Genetics 38:82-92. doi: 10.1007/s10519-007-9173-0.
27. Isoherranen E, Aspi J, Hoikkala A. 1999. Variation and consistency of female preferences for simulated courtship songs in Drosophila virilis. Animal Behaviour 57:619-625. doi: 10.1006/anbe.1998.0981.
28. Kimura K, Hachiya T, Koganezawa M, Tazawa T, Yamamoto D. 2008. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59:759-769. doi: 10.1016/j.neuron.2008.06.007.
29. Kovach KA, Hall ML, Vehrencamp SL, Mennill DJ. 2014. Timing isn't everything: responses of three tropical wrens to coordinated duets, uncoordinated duets, and alternating solos. Animal Behaviour 95:101-109. doi: 10.1016/j. anbehav.2014.06.012.
30. Kulahci IG, Dornhaus A, Papaj DR. 2008. Multimodal signals enhance decision making in foraging bumble-bees. Proceedings. Biological Sciences/The Royal Society 275:797-802. doi: 10.1098/rspb.2007.1176.
31. Kuntz SG, Eisen MB. 2014. Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLOS Genetics 10:e1004293. doi: 10.1371/journal.pgen.1004293.
32. Logue DM, Chalmers C, Gowland H. 2008. The behavioural mechanisms underlying temporal coordination in black-bellied wren duets. Animal Behaviour 75:1803-1808. doi: 10.1016/j.anbehav.2007.10.036.
33. Luo C, Wei C. 2015. Intraspecific sexual mimicry for finding females in a cicada: males produce 'female sounds' to gain reproductive benefit. Animal Behaviour 102:69-76. doi: 10.1016/j.anbehav.2015.01.013.
34. Mann NI, Dingess KA, Slater PJ. 2006. Antiphonal four-part synchronized chorusing in a Neotropical wren. Biology Letters 2:1-4. doi: 10.1098/rsbl.2005.0373.
35. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS. 2005. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436:395-400. doi: 10.1038/nature03859.
36. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB. 2014. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156:1060-1071. doi: 10.1016/j.cell.2013.12.044.
37. Mineault PJ, Barthelme S, Pack CC. 2009. Improved classification images with sparse priors in a smooth basis. Journal of Vision 9:17.1-17.24. doi: 10.1167/9.10.17.
38. Mirjany M, Preuss T, Faber DS. 2011. Role of the lateral line mechanosensory system in directionality of goldfish auditory evoked escape response. The Journal of Experimental Biology 214:3358-3367. doi: 10.1242/jeb.052894.
39. Murthy M, Turner GC. 2010. In vivo whole-cell recordings in the Drosophila brain. In: Zhang B, Freeman MR, Waddell S, editors. Drosophila Neurobiology: A Laboratory Manual: CSHL Press.
40. Narins PM, Grabul DS, Soma KK, Gaucher P, Hödl W. 2005. Cross-modal integration in a dart-poison frog. Proceedings of the National Academy of Sciences of USA 102:2425-2429. doi: 10.1073/pnas.0406407102.
41. Odom KJ, Hall ML, Riebel K, Omland KE, Langmore NE. 2014. Female song is widespread and ancestral in songbirds. Nature Communications 5:3379. doi: 10.1038/ncomms4379.
42. Pan Y, Baker BS. 2014. Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila. Cell 156:236-248. doi: 10.1016/j.cell.2013.11.041.
43. Park JH, Kwon JY. 2011. A systematic analysis of Drosophila gustatory receptor gene expression in abdominal neurons which project to the central nervous system. Molecullar Cells 32:375-381. doi: 10.1007/s10059-011-0128-1.
44. Partan SR, Marler P. 2005. Issues in the classification of multimodal communication signals. The American Naturalist 166:231-245. doi: 10.1086/431246.
45. Ramdya P, Lichocki P, Cruchet S, Frisch L, Tse W, Floreano D, Benton R. 2014. Mechanosensory interactions drive collective behaviour in Drosophila. Nature 519:233-236. doi: 10.1038/nature14024.
46. Raposo D, Sheppard JP, Schrater PR, Churchland AK. 2012. Multisensory decision-making in rats and humans. The Journal of Neuroscience 32:3726-3735. doi: 10.1523/JNEUROSCI.4998-11.2012.
47. Rheinlaender J, Hardt M, Robinson DJ. 1986. The directional sensitivity of a bush cricket ear: a behavioural and neurophysiological study of Leptophyes punctatissima. Physiological Entomology 11:309-316. doi: 10.1111/j. 1365-3032.1986.tb00418.x.
48. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF. 2010. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nature Neuroscience 13:458-466. doi: 10.1038/nn.2515.
49. Ritchie MG, Townhill RM, Hoikkala A. 1998. Female preference for fly song: playback experiments confirm the targets of sexual selection. Animal Behaviour 56:713-717. doi: 10.1006/anbe.1998.0799.
50. Rogers SM, Matheson T, Despland E, Dodgson T, Burrows M, Simpson SJ. 2003. Mechanosensory-induced behavioural gregarization in the desert locust Schistocerca gregaria. The Journal of Experimental Biology 206: 3991-4002. doi: 10.1242/jeb.00648.
51. Rowe C. 1999. Receiver psychology and the evolution of multicomponent signals. Animal Behaviour 58:921-931. doi: 10.1006/anbe.1999.1242.
52. Satokangas P, Liimatainen JO, Hoikkala A. 1994. Songs produced by the females of the Drosophila virilis group of species. Behavior Genetics 24:263-272. doi: 10.1007/BF01067193.
53. Simpson JH. 2009. Mapping and manipulating neural circuits in the fly brain. Advances in Genetics 65:79-143. doi: 10.1016/S0065-2660(09)65003-3.
54. Spieth HT. 1966. Drosophilid mating behavior: the behaviour of decapitated females. Animal Behaviour 14: 226-235. doi: 10.1016/S0003-3472(66)80076-3.
55. Suvanto L, Hoikkala A, Liimatainen JO. 1994. Secondary courtship songs and inhibitory songs of Drosophila virilisgroup males. Behavior Genetics 24:85-94. doi: 10.1007/BF01067932.
56. Suvanto L, Liimatainen JO, Hoikkala A. 1999. Variability and evolvability of male song characters in Drosophila montana populations. Hereditas 130:13-18. doi: 10.1111/j.1601-5223.1999.00013.x.
57. Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K. 2012. Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 149:1140-1151. doi: 10.1016/j.cell.2012.03.045.
58. Tobias ML, Viswanathan SS, Kelley DB. 1998. Rapping, a female receptive call, initiates male-female duets in the South African clawed frog. Proceedings of the National Academy of Sciences of USA 95:1870-1875. doi: 10. 1073/pnas.95.4.1870.
59. Usui-Aoki K, Mikawa Y, Yamamoto D. 2005. Species-specific patterns of sexual dimorphism in the expression of fruitless protein, a neural musculinizing factor in Drosophila. Journal of Neurogenetics 19:109-121. doi: 10.1080/ 01677060591007191.
60. Vedenina VY, Ivanova TI, Lazebny OE. 2013. Analysis of courtship behavior in closely related species of Drosophila virilis group: a new approach arises new question. Journal of Insect Behavior 26:402-415. doi: 10.1007/s10905-012-9359-z.
61. Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. 1997. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147:1107-1130.
62. Villella A, Hall JC. 2008. Neurogenetics of courtship and mating in Drosophila. Advances in Genetics 62:67-184. doi: 10.1016/S0065-2660(08)00603-2.
63. von Philipsborn AC, Liu T, Yu JY, Masser C, Bidaye SS, Dickson BJ. 2011. Neuronal control of Drosophila courtship song. Neuron 69:509-522. doi: 10.1016/j.neuron.2011.01.011.
64. Vuoristo M, Isoherranen E, Hoikkala A. 1996. Female wing spreading as acceptance signal in the Drosophila virilis group of species. Journal of Insect Behavior 9:505-516. doi: 10.1007/BF02214026.
65. Wiens JJ. 2001. Widespread loss of sexually selected traits: how the peacock lost its spots. Journal of Evolutionary Biology 16:517-523. doi: 10.1016/S0169-5347(01)02217-0.
66. Yamamoto D, Usui-Aoki K, Shima S. 2004. Male-specific expression of the fruitless protein is not common to all Drosophila species. Genetica 120:267-272. doi: 10.1023/B:GENE.0000017648.15038.84.
67. Yapici N, Kim YJ, Ribeiro C, Dickson BJ. 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451:33-37. doi: 10.1038/nature06483.