1932

Abstract

Across the animal kingdom, social interactions rely on sound production and perception. From simple cricket chirps to more elaborate bird songs, animals go to great lengths to communicate information critical for reproduction and survival via acoustic signals. Insects produce a wide array of songs to attract a mate, and the intended receivers must differentiate these calls from competing sounds, analyze the quality of the sender from spectrotemporal signal properties, and then determine how to react. Insects use numerically simple nervous systems to analyze and respond to courtship songs, making them ideal model systems for uncovering the neural mechanisms underlying acoustic pattern recognition. We highlight here how the combination of behavioral studies and neural recordings in three groups of insects—crickets, grasshoppers, and fruit flies—reveals common strategies for extracting ethologically relevant information from acoustic patterns and how these findings might translate to other systems.

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2019-07-08
2024-10-05
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Literature Cited

  1. Alder TB, Rose GJ. 1998. Long-term temporal integration in the anuran auditory system. Nat. Neurosci. 1:6519–23
    [Google Scholar]
  2. Arthur BJ, Sunayama-Morita T, Coen P, Murthy M, Stern DL 2013. Multi-channel acoustic recording and automated analysis of Drosophila courtship songs. BMC Biol 11:111
    [Google Scholar]
  3. Atkins G, Ligman S, Burghardt F, Stout JF 1984. Changes in phonotaxis by the female cricket Acheta domesticus L. after killing identified acoustic interneurons. J. Comp. Physiol. A 154:6795–804
    [Google Scholar]
  4. Azevedo AW, Wilson RI. 2017. Active mechanisms of vibration encoding and frequency filtering in central mechanosensory neurons. Neuron 96:446–60.E9
    [Google Scholar]
  5. Baker CA, Carlson BA. 2014. Short-term depression, temporal summation, and onset inhibition shape interval tuning in midbrain neurons. J. Neurosci. 34:4314272–87
    [Google Scholar]
  6. Baker CA, Ma L, Casareale CR, Carlson BA 2016. Behavioral and single-neuron sensitivity to millisecond variations in temporally patterned communication signals. J. Neurosci. 36:348985–9000
    [Google Scholar]
  7. Bennet-Clark HC, Ewing AW. 1969. Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster. Anim. Behav 17:4755–59
    [Google Scholar]
  8. Bhavsar MB, Heinrich R, Stumpner A 2015. Multielectrode recordings from auditory neurons in the brain of a small grasshopper. J. Neurosci. Methods 256:63–73
    [Google Scholar]
  9. Blankers T, Hennig RM, Gray DA 2015. Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. J. Evol. Biol. 28:3630–41
    [Google Scholar]
  10. Bradbury JW, Vehrencamp SL. 2011. Principles of Animal Communication Sunderland, MA: Sinauer Assoc. Inc. , 2nd ed..
    [Google Scholar]
  11. Bussell JJ, Yapici N, Zhang SX, Dickson BJ, Vosshall LB 2014. Abdominal-B neurons control Drosophila virgin female receptivity. Curr. Biol. 24:141584–95
    [Google Scholar]
  12. Cande J, Namiki S, Qiu J, Korff W, Card GM et al. 2018. Optogenetic dissection of descending behavioral control in Drosophila. . eLife 7:e34275
    [Google Scholar]
  13. Carlson BA, Hopkins CD. 2004. Stereotyped temporal patterns in electrical communication. Anim. Behav. 68:4867–78
    [Google Scholar]
  14. Chaverra-Rodriguez D, Macias VM, Hughes GL, Pujhari S, Suzuki Y et al. 2018. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9:3008
    [Google Scholar]
  15. Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL et al. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:7458295–300
    [Google Scholar]
  16. Clemens J, Coen P, Roemschied F, Pereira T, Mazumder D et al. 2018a. Discovery of a new song mode in Drosophila reveals hidden structure in the sensory and neural drivers of behavior. Curr. Biol. 28:2400–12.E6
    [Google Scholar]
  17. Clemens J, Deutsch D, Thiberge SY, Murthy M 2018b. Shared song object detector neurons in Drosophila male and female brains drive divergent, sex-specific behaviors. bioRxiv 366765. https://doi.org/10.1101/366765
    [Crossref]
  18. Clemens J, Girardin CC, Coen P, Guan X-J, Dickson BJ, Murthy M 2015. Connecting neural codes with behavior in the auditory system of Drosophila. . Neuron 87:61332–43
    [Google Scholar]
  19. Clemens J, Hennig RM. 2013. Computational principles underlying the recognition of acoustic signals in insects. J. Comput. Neurosci. 35:175–85
    [Google Scholar]
  20. Clemens J, Krämer S, Ronacher B 2014. Asymmetrical integration of sensory information during mating decisions in grasshoppers. PNAS 111:4616562–67
    [Google Scholar]
  21. Clemens J, Kutzki O, Ronacher B, Schreiber S, Wohlgemuth S 2011. Efficient transformation of an auditory population code in a small sensory system. PNAS 108:3313812–17
    [Google Scholar]
  22. Coen P, Clemens J, Weinstein AJ, Pacheco DA, Deng Y, Murthy M 2014. Dynamic sensory cues shape song structure in Drosophila. . Nature 507:7491233–37
    [Google Scholar]
  23. Coen P, Murthy M. 2016. Singing on the fly: sensorimotor integration and acoustic communication in Drosophila. Curr. Opin. Neurobiol 38:38–45
    [Google Scholar]
  24. Coen P, Xie M, Clemens J, Murthy M 2016. Sensorimotor transformations underlying variability in song intensity during Drosophila courtship. Neuron 89:3629–44
    [Google Scholar]
  25. Cowling DE, Burnet B. 1981. Courtship songs and genetic control of their acoustic characteristics in sibling species of the Drosophila melanogaster subgroup. Anim. Behav. 29:3924–35
    [Google Scholar]
  26. Creutzig F, Benda J, Wohlgemuth S, Stumpner A, Ronacher B, Herz AVM 2010. Timescale-invariant pattern recognition by feedforward inhibition and parallel signal processing. Neural Comput 22:1493–510
    [Google Scholar]
  27. Creutzig F, Wohlgemuth S, Stumpner A, Benda J, Ronacher B, Herz AVM 2009. Timescale-invariant representation of acoustic communication signals by a bursting neuron. J. Neurosci. 29:82575–80
    [Google Scholar]
  28. Crossley SA, Bennet-Clark HC, Evert HT 1995. Courtship song components affect male and female Drosophila differently. Anim. Behav. 50:3827–39
    [Google Scholar]
  29. Eberl DF, Duyk GM, Perrimon N 1997. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. . PNAS 94:14837–42
    [Google Scholar]
  30. Edwards CJ, Alder TB, Rose GJ 2002. Auditory midbrain neurons that count. Nat. Neurosci. 5:10934–36
    [Google Scholar]
  31. Eisenberg JF, Kleiman DG. 1972. Olfactory communication in mammals. Annu. Rev. Ecol. Syst. 3:1–32
    [Google Scholar]
  32. Fellers GM. 1979. Aggression, territoriality, and mating behaviour in North American treefrogs. Anim. Behav. 27:107–19
    [Google Scholar]
  33. Fettiplace R, Fuchs PA. 1999. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 61:809–34
    [Google Scholar]
  34. Finck J, Kuntze J, Ronacher B 2016. Chemical cues from females trigger male courtship behaviour in grasshoppers. J. Comp. Physiol. A 202:5337–45
    [Google Scholar]
  35. Franconville R, Beron C, Jayaraman V 2018. Building a functional connectome of the Drosophila central complex. eLife 7:e37017
    [Google Scholar]
  36. George AA, Lyons-Warren AM, Ma X, Carlson BA 2011. A diversity of synaptic filters are created by temporal summation of excitation and inhibition. J. Neurosci. 31:4114721–34
    [Google Scholar]
  37. Goel A, Buonomano DV. 2014. Timing as an intrinsic property of neural networks: evidence from in vivo and in vitro experiments. Philos. Trans. R. Soc. B Biol. Sci. 369:163720120460
    [Google Scholar]
  38. Göpfert MC, Hennig RM. 2016. Hearing in insects. Annu. Rev. Entomol. 61:257–76
    [Google Scholar]
  39. Gray DA, Gabel E, Blankers T, Hennig RM 2016. Multivariate female preference tests reveal latent perceptual biases. Proc. Biol. Sci. 283:184220161972
    [Google Scholar]
  40. Grobe B, Rothbart MM, Hanschke A, Hennig RM 2012. Auditory processing at two time scales by the cricket Gryllusbimaculatus. J. Exp. Biol 215:101681–90
    [Google Scholar]
  41. Halfwerk W, Jones PL, Taylor RC, Ryan MJ, Page RA 2014. Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display. Science 343:6169413–16
    [Google Scholar]
  42. Hartbauer M, Römer H. 2014. From microseconds to seconds and minutes—time computation in insect hearing. Front. Physiol. 5:138
    [Google Scholar]
  43. Hedwig BG. 2016. Sequential filtering processes shape feature detection in crickets: a framework for song pattern recognition. Front. Physiol. 7:46
    [Google Scholar]
  44. Hedwig BG, Poulet JFA. 2004. Complex auditory behaviour emerges from simple reactive steering. Nature 430:7001781–85
    [Google Scholar]
  45. Hildebrandt KJ, Benda J, Hennig RM 2015. Computational themes of peripheral processing in the auditory pathway of insects. J. Comp. Physiol. A 201:139–50
    [Google Scholar]
  46. Hill PSM. 2001. Vibration and animal communication: a review. Integr. Comp. Biol. 41:51135–42
    [Google Scholar]
  47. Hopkins CD. 1988. Neuroethology of electric communication. Annu. Rev. Neurosci. 11:497–535
    [Google Scholar]
  48. Imaizumi K, Pollack GS. 2005. Central projections of auditory receptor neurons of crickets. J. Comp. Neurol. 493:3439–47
    [Google Scholar]
  49. Inagaki HK, Jung Y, Hoopfer ED, Wong AM, Mishra N et al. 2014. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11:3325–32
    [Google Scholar]
  50. Ishikawa Y, Okamoto N, Nakamura M, Kim H, Kamikouchi A 2017. Anatomic and physiologic heterogeneity of subgroup-A auditory sensory neurons in fruit flies. Front. Neural Circuits 11:46
    [Google Scholar]
  51. Jonsson T, Kravitz EA, Heinrich R 2011. Sound production during agonistic behavior of male Drosophila melanogaster. . Fly 5:129–38
    [Google Scholar]
  52. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A et al. 2009. The neural basis of Drosophila gravity-sensing and hearing. Nature 458:7235165–71
    [Google Scholar]
  53. Kamikouchi A, Shimada T, Ito K 2006. Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J. Comp. Neurol 499:3317–56
    [Google Scholar]
  54. Kanwal JS, Rauschecker JP. 2007. Auditory cortex of bats and primates: managing species-specific calls for social communication. Front. Biosci. 12:4621–40
    [Google Scholar]
  55. Klappert K, Reinhold K. 2003. Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippusbiguttulus. Anim. Behav 65:1225–33
    [Google Scholar]
  56. Kohashi T, Carlson BA. 2014. A fast BK-type KCa current acts as a postsynaptic modulator of temporal selectivity for communication signals. Front. Cell. Neurosci. 8:286
    [Google Scholar]
  57. Kostarakos K, Hedwig B. 2012. Calling song recognition in female crickets: Temporal tuning of identified brain neurons matches behavior. J. Neurosci. 32:289601–12
    [Google Scholar]
  58. Kowalski S, Aubin T, Martin J-R 2004. Courtship song in Drosophila melanogaster: a differential effect on male-female locomotor activity. Can. J. Zool. 82:81258–66
    [Google Scholar]
  59. Kriegbaum H. 1989. Female choice in the grasshopper Chorthippus biguttulus. . Naturwissenschaften 76:281–82
    [Google Scholar]
  60. Lai JS-Y, Lo S-J, Dickson BJ, Chiang A-S 2012. Auditory circuit in the Drosophila brain. PNAS 109:72607–12
    [Google Scholar]
  61. Li X, Ishimoto H, Kamikouchi A 2018. Auditory experience controls the maturation of song discrimination and sexual response in Drosophila. . eLife 7:e34348
    [Google Scholar]
  62. Libersat F, Murray JA, Hoy RR 1994. Frequency as a releaser in the courtship song of two crickets, Gryllus bimaculatus (de Geer) and Teleogryllus oceanicus: a neuroethological analysis. J. Comp. Physiol. A 174:4485–94
    [Google Scholar]
  63. Mann K, Gallen CL, Clandinin TR 2017. Whole-brain calcium imaging reveals an intrinsic functional network in Drosophila. Curr. Biol 27:152389–96.e4
    [Google Scholar]
  64. Markow TA, O'Grady PM. 2005. Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots. Annu. Rev. Genet. 39:263–91
    [Google Scholar]
  65. Marsat G, Pollack GS. 2005. Effect of the temporal pattern of contralateral inhibition on sound localization cues. J. Neurosci. 25:266137–44
    [Google Scholar]
  66. Matsuo E, Seki H, Asai T, Morimoto T, Miyakawa H et al. 2016. Organization of projection neurons and local neurons of the primary auditory center in the fruit fly Drosophila melanogaster. J. Comp. Neurol 524:61099–164
    [Google Scholar]
  67. Matsuo E, Yamada D, Ishikawa Y, Asai T, Ishimoto H, Kamikouchi A 2014. Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston's organ of the fruit fly. Front. Physiol. 5:179
    [Google Scholar]
  68. Meckenhäuser G, Hennig RM, Nawrot MP 2013. Critical song features for auditory pattern recognition in crickets. PLOS ONE 8:2e55349
    [Google Scholar]
  69. Meyer J, Elsner N. 1996. How well are frequency sensitivities of grasshopper ears tuned to species-specific song spectra. ? J. Exp. Biol. 199:71631–42
    [Google Scholar]
  70. Nolen TG, Hoy RR. 1984. Initiation of behavior by single neurons: the role of behavioral context. Science 226:4677992–94
    [Google Scholar]
  71. Osorio D, Vorobyev M. 2008. A review of the evolution of animal colour vision and visual communication signals. Vision Res 48:202042–51
    [Google Scholar]
  72. Ostrowski TD, Sradnick J, Stumpner A, Elsner N 2009. The elaborate courtship behavior of Stenobothrus clavatus (Acrididae: Gomphocerinae). J. Orthoptera Res. 18:2171–82
    [Google Scholar]
  73. Otte D. 1992. Evolution of cricket songs. J. Orthoptera Res. 1:25–49
    [Google Scholar]
  74. Patella P, Wilson RI. 2018. Functional maps of mechanosensory features in the Drosophila brain. Curr. Biol. 28:81189–203.e5
    [Google Scholar]
  75. Pollack GS, Hedwig B. 2017. The cricket auditory pathway: neural processing of acoustic signals. The Cricket as a Model Organism HW Horch, T Mito, A Popadić, H Ohuchi, S Noji 155–67 Tokyo: Springer
    [Google Scholar]
  76. Pollack GS, Mason AC, Popper AN, Fay RR, eds. 2016. Insect Hearing. Switz: Springer
    [Google Scholar]
  77. Poremba A, Bigelow J, Rossi B 2013. Processing of communication sounds: contributions of learning, memory, and experience. Hear. Res. 305:31–44
    [Google Scholar]
  78. Poulet JFA, Hedwig B. 2005. Auditory orientation in crickets: pattern recognition controls reactive steering. PNAS 102:4315665–69
    [Google Scholar]
  79. Reichert MS, Gerhardt HC. 2014. Behavioral strategies and signaling in interspecific aggressive interactions in gray tree frogs. Behav. Ecol. 25:3520–30
    [Google Scholar]
  80. Riabinina O, Dai M, Duke T, Albert JT 2011. Active process mediates species-specific tuning of Drosophila ears. Curr. Biol. 21:8658–64
    [Google Scholar]
  81. Römer H, Marquart V. 1984. Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J. Comp. Physiol. A 155:2249–62
    [Google Scholar]
  82. Römer H, Rheinlaender J, Dronse R 1981. Intracellular studies on auditory processing in the metathoracic ganglion of the locust. J. Comp. Physiol. 144:3305–12
    [Google Scholar]
  83. Ronacher B. 2014. Processing of species-specific signals in the auditory pathway of grasshoppers. Insect Hearing and Acoustic Communication: Animal Signals and Communication, Vol. 1 B Hedwig 185–204 Berlin/Heidelberg: Springer
    [Google Scholar]
  84. Ronacher B, Hennig RM, Clemens J 2015. Computational principles underlying recognition of acoustic signals in grasshoppers and crickets. J. Comp. Physiol. A 201:161–71
    [Google Scholar]
  85. Ronacher B, Stumpner A. 1988. Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron. J. Comp. Physiol. A 163:4517–23
    [Google Scholar]
  86. Rose GJ. 2014. Time computations in anuran auditory systems. Front. Physiol. 5:206
    [Google Scholar]
  87. Rose GJ. 2017. The numerical abilities of anurans and their neural correlates: insights from neuroethological studies of acoustic communication. Philos. Trans. R. Soc. Lond. B Biol. Sci. 373:174020160512
    [Google Scholar]
  88. Rose GJ, Brenowitz EA. 2002. Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls. Anim. Behav. 63:61183–90
    [Google Scholar]
  89. Rose GJ, Capranica RR. 1983. Temporal selectivity in the central auditory system of the leopard frog. Science 219:45881087–89
    [Google Scholar]
  90. Rothbart MM, Hennig RM. 2012. The Steppengrille (Gryllus spec./assimilis): selective filters and signal mismatch on two time scales. PLOS ONE 7:9e43975
    [Google Scholar]
  91. Rybak F, Sureau G, Aubin T 2002. Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster. Proc. R. Soc. B 269:1492695–701
    [Google Scholar]
  92. Schmidt A, Ronacher B, Hennig RM 2008. The role of frequency, phase and time for processing of amplitude modulated signals by grasshoppers. J. Comp. Physiol. A 194:3221–33
    [Google Scholar]
  93. Schneider DM, Woolley SMN. 2013. Sparse and background-invariant coding of vocalizations in auditory scenes. Neuron 79:1141–52
    [Google Scholar]
  94. Schöneich S, Kostarakos K, Hedwig B 2015. An auditory feature detection circuit for sound pattern recognition. Sci. Adv. 1:8e1500325
    [Google Scholar]
  95. Seeholzer LF, Seppo M, Stern DL, Ruta V 2018. Evolution of a central neural circuit underlies Drosophila mate preferences. Nature 559:7715564–69
    [Google Scholar]
  96. Shirangi TR, Stern DL, Truman JW 2013. Motor control of Drosophila courtship song. Cell Rep 5:3678–86
    [Google Scholar]
  97. Stern DL, Crocker J, Ding Y, Frankel N, Kappes G et al. 2017. Genetic and transgenic reagents for Drosophila simulans, D. mauritiana, D. yakuba, D. santomea, and D. virilis. . G3 7:41339–47
    [Google Scholar]
  98. Stumpner A. 2002. A species-specific frequency filter through specific inhibition, not specific excitation. J. Comp. Physiol. A 188:3239–48
    [Google Scholar]
  99. Stumpner A, Atkins G, Stout JF 1995. Processing of unilateral and bilateral auditory inputs by the ON1 and L1 interneurons of the cricket Acheta domesticus and comparison to other cricket species. J. Comp. Physiol. A 177:379–88
    [Google Scholar]
  100. Stumpner A, Ronacher B. 1991. Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus: I. Morphological and physiological characterization. J. Exp. Biol. 158:3391–410
    [Google Scholar]
  101. Stumpner A, Ronacher B. 1994. Neurophysiological aspects of song pattern recognition and sound localization in grasshoppers. Integr. Comp. Biol. 34:6696–705
    [Google Scholar]
  102. Sun D, Guo Z, Liu Y, Zhang Y 2017. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Front. Physiol. 8:608
    [Google Scholar]
  103. Talyn BC, Dowse HB. 2004. The role of courtship song in sexual selection and species recognition by female Drosophila melanogaster. Anim. Behav 68:51165–80
    [Google Scholar]
  104. Tootoonian S, Coen P, Kawai R, Murthy M 2012. Neural representations of courtship song in the Drosophila brain. J. Neurosci. 32:3787–98
    [Google Scholar]
  105. Tuttle MD, Ryan MJ. 1981. Bat predation and the evolution of frog vocalizations in the neotropics. Science 214:4521677–78
    [Google Scholar]
  106. Vaughan AG, Zhou C, Manoli DS, Baker BS 2014. Neural pathways for the detection and discrimination of conspecific song in D. melanogaster. Curr. Biol 24:101039–49
    [Google Scholar]
  107. Versteven M, Vanden Broeck L, Geurten B, Zwarts L, Decraecker L et al. 2017. Hearing regulates Drosophila aggression. PNAS 114:81958–63
    [Google Scholar]
  108. von Helversen D. 1972. Gesang des Männchens und Lautschema des Weibchens bei der Feldheuschrecke Chorthippus biguttulus (Orthoptera, Acrididae). J. Comp. Physiol. 81:4381–422
    [Google Scholar]
  109. von Helversen D, von Helversen O 1997. Recognition of sex in the acoustic communication of the grasshopper Chorthippus biguttulus (Orthoptera, Acrididae). J. Comp. Physiol. A 180:4373–86
    [Google Scholar]
  110. von Schilcher F. 1976. The role of auditory stimuli in the courtship of Drosophila melanogaster. Anim. Behav 24:118–26
    [Google Scholar]
  111. Windmill JFC, Jackson JC. 2016. Mechanical specializations of insect ears. See Pollack et al. 2016 125–57
  112. Wohlers DW, Huber F. 1982. Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket, Gryllus campestris L. J. Comp. Physiol. 146:2161–73
    [Google Scholar]
  113. Woolley SMN, Portfors CV. 2013. Conserved mechanisms of vocalization coding in mammalian and songbird auditory midbrain. Hear. Res. 305:45–56
    [Google Scholar]
  114. Wyttenbach RA, May ML, Hoy RR 1996. Categorical perception of sound frequency by crickets. Science 273:52811542–44
    [Google Scholar]
  115. Yamada D, Ishimoto H, Li X, Kohashi T, Ishikawa Y, Kamikouchi A 2018. GABAergic local interneurons shape female fruit fly response to mating songs. J. Neurosci. 38:4329–47
    [Google Scholar]
  116. Yang HH, St-Pierre F. 2016. Genetically encoded voltage indicators: opportunities and challenges. J. Neurosci. 36:39977–89
    [Google Scholar]
  117. Yoon J, Matsuo E, Yamada D, Mizuno H, Morimoto T et al. 2013. Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila. . PLOS ONE 8:9e74289
    [Google Scholar]
  118. Yorozu S, Wong A, Fischer BJ, Dankert H, Kernan MJ et al. 2009. Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458:7235201–5
    [Google Scholar]
  119. Zheng Z, Lauritzen JS, Perlman E, Robinson CG, Nichols M et al. 2018. A complete electron microscopy volume of the brain of adult Drosophila melanogaster. . Cell 174:3730–43.E22
    [Google Scholar]
  120. Zhou C, Franconville R, Vaughan AG, Robinett CC, Jayaraman V, Baker BS 2015. Central neural circuitry mediating courtship song perception in male Drosophila. . eLife 4:e08477
    [Google Scholar]
  121. Zhou C, Pan Y, Robinett CC, Meissner GW, Baker BS 2014. Central brain neurons expressing doublesex regulate female receptivity in Drosophila. . Neuron 83:1149–63
    [Google Scholar]
  122. Zuk M, Kolluru GR. 1998. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73:415–38
    [Google Scholar]
  123. Zuk M, Rebar D, Scott SP 2008. Courtship song is more variable than calling song in the field cricket Teleogryllusoceanicus. Anim. Behav 76:31065–71
    [Google Scholar]
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