Female mice ultrasonically interact with males during courtship displays

eLife

Volumn 4, Issue MAY, 2015, Pages 1-24

  Neunuebel, Joshua P ^a,b   Taylor, Adam L ^a   Arthur, Ben J ^a   Roian Egnor, S E ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL TISSUE; ARTICLE; COURTSHIP; CYTODIAGNOSIS; ESTRUS; FEMALE; INTERPERSONAL COMMUNICATION; LAVAGE; LIGHT DARK CYCLE; MALE; MATHEMATICAL ANALYSIS; MEASUREMENT PRECISION; MICROPHONE; NONHUMAN; PHYSICAL PARAMETERS; SCORING SYSTEM; SEXUAL BEHAVIOR; SIGNAL DETECTION; SOCIAL INTERACTION; ULTRASONIC VOCALIZATION; VOCALIZATION; ANIMAL; C57BL MOUSE; DEVICES; MOUSE; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; SEX DIFFERENCE; SOCIAL BEHAVIOR; ULTRASOUND;

MUS;

ANIMALS; COURTSHIP; FEMALE; MALE; MICE; MICE, INBRED C57BL; SEX FACTORS; SOCIAL BEHAVIOR; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 84930620321     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06203     Document Type: Article

References (87)

1. Adolphs R. 2010. Conceptual challenges and directions for social neuroscience. Neuron 65:752-767. doi: 10.1016/ j.neuron.2010.03.006.
2. Akre KL, Ryan MJ. 2011. Female túngara frogs elicit more complex mating signals from males. Behavioral Ecology 22:846-853. doi: 10.1093/beheco/arr065.
3. Anderson PK. 1961. Density, social structure, and nonsocial environment in house-mouse populations and the implications for regulation of numbers. Transactions of the New York Academy of Sciences 23:447-451. doi: 10. 1111/j.2164-0947.1961.tb01373.x.
4. BarthelemyM, Gourbal BE, Gabrion C, Petit G. 2004. Influence of the female sexual cycle on BALB/c mouse calling behaviour during mating. Die Naturwissenschaften 91:135-138. doi: 10.1007/s00114-004-0501-4.
5. Beach FA. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior 7: 105-138. doi: 10.1016/0018-506X(76)90008-8.
6. Bean NY, Nunez AA, Conner R. 1981. Effects of medial preoptic lesions on male mouse ultrasonic vocalizations and copulatory behavior. Brain Research Bulletin 6:109-112. doi: 10.1016/S0361-9230(81)80033-0.
7. Behr O, von Helversen O. 2004. Bat serenades-complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behavioral Ecology and Sociobiology 56:106-115. doi: 10.1007/s00265-004-0768-7.
8. Bentley GE, Wingfield JC, Morton ML, Ball GF. 2000. Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Hormones and Behavior 37:179-189. doi: 10.1006/hbeh. 2000.1573.
9. Berry RJ, Bronson FH. 1992. Life history and bioeconomy of the house mouse. Biological Reviews of the Cambridge Philosophical Society 67:519-550. doi: 10.1111/j.1469-185X.1992.tb01192.x.
10. Blank DA, Ruckstuhl K, Yang W. 2014. Roaring function in male goitered gazelles. Behavioural Processes 106: 152-159. doi: 10.1016/j.beproc.2014.05.009.
11. Blumstein DT, Mennill DJ, Clemins P, Girod L, Yao K, Patricelli G, Deppe JL, Krakauer AH, Clark C, Cortopassi KA, Sean F Hanser, Brenda McCowan, Andreas M Ali, Alexander NG Kirschel. 2011. Acoustic monitoring in terrestrial environments using microphone arrays: applications, technological considerations and prospectus. Journal of Applied Ecology 48:758-767. doi: 10.1111/j.1365-2664.2011.01993.x.
12. Bradbury JW, Vehrencamp SL. 1998. Principles of animal communication. 2nd edition. Sunderland, Massachusetts: Sinauer Associates, Inc.
13. Celis-Murillo A, Deppe JL, Allen MF. 2009. Using soundscape recordings to estimate bird species abundance, richness, and composition. Journal of Field Ornithology 80:64-78. doi: 10.1111/j.1557-9263.2009.00206.x.
14. Chabout J, Serreau P, Ey E, Bellier L, Aubin T, Bourgeron T, Granon S. 2012. Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLOS ONE 7: e29401. doi: 10.1371/journal.pone.0029401.
15. Charlton BD, Reby D. 2011. Context-related acoustic variation in male fallow deer (Dama dama) groans. PLOS ONE 6:e21066. doi: 10.1371/journal.pone.0021066.
16. Chiu C, Reddy PV, Xian W, Krishnaprasad PS, Moss CF. 2010. Effects of competitive prey capture on flight behavior and sonar beam pattern in paired big brown bats, Eptesicus fuscus. The Journal of Experimental Biology 213: 3348-3356. doi: 10.1242/jeb.044818.
17. Choi H, Park S, Kim D. 2011. Two genetic loci control syllable sequences of ultrasonic courtship vocalizations in inbred mice. BMC Neuroscience 12:104. doi: 10.1186/1471-2202-12-104.
18. 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.
19. Coleman SW, Patricelli GL, Borgia G. 2004. Variable female preferences drive complex male displays. Nature 428: 742-745. doi: 10.1038/nature02419.
20. Collier TC, Blumstein DT, Girod L, Taylor CE. 2010. Is alarm calling risky? Marmots avoid calling from risky places. Ethology 116:1171-1178. doi: 10.1111/j.1439-0310.2010.01830.x.
21. D'Amato FR, Moles A. 2001. Ultrasonic vocalizations as an index of social memory in female mice. Behavioral Neuroscience 115:834-840. doi: 10.1037/0735-7044.115.4.834.
22. Ficken MS, Weise CM, Reinartz JA. 1987. A complex vocalization of the Black-capped Chickadee. II. Repertoires, dominance and dialects. The Condor 89:500-509. doi: 10.2307/1368640.
23. Fitzsimmons LP, Bertram SM. 2013. Playing to an audience: the social environment influences aggression and victory displays. Biology Letters 9:20130449. doi: 10.1098/rsbl.2013.0449.
24. Floody OR, Pfaff DW, Lewis CD. 1977. Communication among hamsters by high-frequency acoustic signals: II. Determinants of calling by females and males. Journal of Comparative and Physiological Psychology 91:807-819. doi: 10.1037/h0077361.
25. Garamszegi LZ, Pavlova DZ, Eens M, Møller AP. 2007. The evolution of song in female birds in Europe. Behavioral Ecology 18:86-96. doi: 10.1093/beheco/arl047.
26. Grosenick L, Clement TS, Fernald RD. 2007. Fish can infer social rank by observation alone. Nature 445:429-432. doi: 10.1038/nature05511.
27. Hall JC. 1994. The mating of a fly. Science 264:1702-1714. doi: 10.1126/science.8209251.
28. Hall M. 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.
29. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J. 2009. Female mice respond to male ultrasonic 'songs' with approach behaviour. Biology Letters 5:589-592. doi: 10.1098/rsbl.2009.0317.
30. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J. 2012a. The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences. PLOS ONE 7:e41133. doi: 10.1371/journal.pone.0041133.
31. Hammerschmidt K, Reisinger E, Westekemper K, Ehrenreich L, Strenzke N, Fischer J. 2012b. Mice do not require auditory input for the normal development of their ultrasonic vocalizations. BMC Neuroscience 13:40. doi: 10. 1186/1471-2202-13-40.
32. Hanson JL, Hurley LM. 2012. Female presence and estrous state influence mouse ultrasonic courtship vocalizations. PLOS ONE 7:e40782. doi: 10.1371/journal.pone.0040782.
33. Higham JP, Semple S, MacLarnon A, Heistermann M, Ross C. 2009. Female reproductive signaling, and male mating behavior, in the olive baboon. Hormones and Behavior 55:60-67. doi: 10.1016/j.yhbeh.2008.08.007.
34. Hoffmann F, Musolf K, Penn DJ. 2012. Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiology & Behavior 105:766-771. doi: 10.1016/j. physbeh.2011.10.011.
35. Holy TE, Guo Z. 2005. Ultrasonic songs of male mice. Plos Biology 3:e386. doi: 10.1371/journal.pbio.0030386.
36. Janson CH. 1984. Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). Zeitschrift für Tierpsychologie 65:177-200.
37. Jones RB, Nowell NW. 1989. Aversive potency of urine from dominant and subordinate male laboratory mice (Mus musculus): resolution of a conflict. Aggressive Behavior 15:291-296. doi: 10.1002/ab.2480150404.
38. Kabra M, Robie AA, Rivera-Alba M, Branson S, Branson K. 2013. JAABA: interactive machine learning for automatic annotation of animal behavior. Nature Methods 10:64-67. doi: 10.1038/nmeth.2281.
39. Kalcounis-Rueppell MC, Petric R, Briggs JR, Carney C, Marshall MM, Willse JT, Rueppell O, Ribble DO, Crossland JP. 2010. Differences in ultrasonic vocalizations between wild and laboratory California mice (Peromyscus californicus). PLOS ONE 5:e9705. doi: 10.1371/journal.pone.0009705.
40. Karim BO, Landolfi JA, Christian A, Ricart-Arbona R, Qiu W, McAlonis M, Eyabi PO, Khan KA, Dicello JF, Mann JF, Huso DL. 2003. Estrous cycle and ovarian changes in a rat mammary carcinogenesis model after irradiation, tamoxifen chemoprevention, and aging. Comparative Medicine 53:532-538.
41. Kimchi T, Xu J, Dulac C. 2007. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009-1014. doi: 10.1038/nature06089.
42. Kirschel ANG, Cody ML, Harlow ZT, Promponas VJ, Vallejo EE, Taylor CE. 2011. Territorial dynamics of Mexican Ant-thrushes Formicarius moniliger revealed by individual recognition of their songs. Ibis 153:255-268. doi: 10. 1111/j.1474-919X.2011.01102.x.
43. König B. 1994. Fitness effects of communal rearing in house mice: the role of relatedness versus familiarity. Animal Behaviour 48:1449-1457. doi: 10.1006/anbe.1994.1381.
44. Kowalski S, Aubin T, Martin J-R. 2004. Courtship song in Drosophila melanogaster: a differential effect on male-female locomotor activity. Canadian Journal of Zoology 82:1258-1266. doi: 10.1139/z04-102.
45. Leong KM, Ortolani A Fau - Graham LH, Graham Lh Fau - Savage A, Savage A. 2003. The use of low-frequency vocalizations in African elephant (Loxodonta africana) reproductive strategies. Hormones and Behavior 43: 433-443. doi: 10.1016/S0018-506X(03)00025-4.
46. Maggio JC, Whitney G. 1985. Ultrasonic vocalizing by adult female mice (Mus musculus). Journal of Comparative Psychology 99:420-436. doi: 10.1037/0735-7036.99.4.420.
47. Martinez-Rivera CC, Gerhardt HC. 2008. Advertisement-call modification, male competition and female preference in the bird-voiced treefrog Hyla avivoca. Behav Ecology and Sociobiology 63:195-208.
48. McGill TE. 1962. Sexual behavior in three inbred strains of mice. Behaviour 19:341-350. doi: 10.1163/ 156853962X00087.
49. McIntosh TK, Barfield RJ, Geyer LA. 1978. Ultrasonic vocalisations facilitate sexual behaviour of female rats. Nature 272:163-164. doi: 10.1038/272163a0.
50. Mennill DJ, Burt JM, Fristrup KM, Vehrencamp SL. 2006. Accuracy of an acoustic location system for monitoring the position of duetting songbirds in tropical forest. The Journal of the Acoustical Society of America 119: 2832-2839. doi: 10.1121/1.2184988.
51. Moles A, Costantini F, Garbugino L, Zanettini C, D'Amato FR. 2007. Ultrasonic vocalizations emitted during dyadic interactions in female mice: a possible index of sociability? Behavioural Brain Research 182:223-230. doi: 10. 1016/j.bbr.2007.01.020.
52. Moles A, D'Amato FR. 2000. Ultrasonic vocalization by female mice in the presence of a conspecific carrying food cues. Animal Behaviour 60:689-694. doi: 10.1006/anbe.2000.1504.
53. Montgomerie R, Thornhill R. 1989. Fertility Advertisement in birds: a means of Inciting male-male competition? Ethology 81:209-220.
54. Moore MM. 1985. Nonverbal courtship patterns in women: context and consequences. Ethology and Sociobiology 6:237-247. doi: 10.1016/0162-3095(85)90016-0.
55. Musolf K, Hoffmann F, Penn D. 2010. Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Animal Behaviour 79:757-764. doi: 10.1016/j.anbehav.2009.12.034.
56. Nunez AA, Nyby J, Whitney G. 1978. The effects of testosterone, estradiol, and dihydrotestosterone on male mouse (Mus musculus) ultrasonic vocalizations. Hormones and Behavior 11:264-272. doi: 10.1016/0018-506X(78) 90030-2.
57. Nyby J. 1983. Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. Behavioral and Neural Biology 39:128-134. doi: 10.1016/S0163-1047(83)90722-7.
58. Nyby J, Dizinno GA, Whitney G. 1976. Social status and ultrasonic vocalizations of male mice. Behavioral Biology 18:285-289. doi: 10.1016/S0091-6773(76)92198-2.
59. Nyby J, Wysocki CJ, Whitney G, Dizinno G, Schneider J. 1979. Elicitation of male mouse (Mus musculus) ultrasonic vocalizations: I. Urinary cues. Journal of Comparative and Physiological Psychology 93:957-975. doi: 10.1037/ h0077623.
60. Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson JA, Smithies O, Korach KS, Pfaff DW. 2000. Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO). Proceedings of the National Academy of Sciences of the United States of America 97:14737-14741. doi: 10.1073/pnas.250473597.
61. Ohayon S, Avni O, Taylor AL, Perona P, Roian Egnor SE. 2013. Automated multi-day tracking of marked mice for the analysis of social behaviour. Journal of Neuroscience Methods 219:10-19. doi: 10.1016/j.jneumeth.2013.05.013.
62. Payne KB, Thompson M, Kramer L. 2003. Elephant calling patterns as indicators of group size and composition: the basis for an acoustic monitoring system. African Journal of Ecology 41:99-107. doi: 10.1046/j.1365-2028. 2003.00421.x.
63. Peña D, Prieto F. 2001. Multivariate outlier detection and robust covariance matrix estimation. Technometrics 43: 286-310. doi: 10.1198/004017001316975899.
64. Percival D, Walden A. 1993. Spectral analysis for physical applications, multitaper and conventional univariate techniques. New York, New York: Cambridge University Press.
65. Pomerantz SM, Clemens LG. 1981. Ultrasonic vocalizations in male deer mice (Peromyscus maniculatus bairdi): their role in male sexual behavior. Physiology & Behavior 27:869-872. doi: 10.1016/0031-9384(81)90055-X.
66. Pomerantz SM, Nunez AA, Bean NJ. 1983. Female behavior is affected by male ultrasonic vocalizations in house mice. Physiology & Behavior 31:91-96. doi: 10.1016/0031-9384(83)90101-4.
67. Portfors CV. 2007. Types and functions of ultrasonic vocalizations in laboratory rats and mice. Journal of the American Association for Laboratory Animal Science 46:28-34.
68. Portfors CV, Perkel DJ. 2014. The role of ultrasonic vocalizations in mouse communication. Current Opinion in Neurobiology 28:115-120. doi: 10.1016/j.conb.2014.07.002.
69. Rand AS, Ryan MJ. 1981. The adaptive significance of a complex vocal repertoire in a Neotropical frog. Zeitschrift für Tierpsychologie 57:209-214. doi: 10.1111/j.1439-0310.1981.tb01923.x.
70. Rotschafer SE, Trujillo MS, Dansie LE, Ethell IM, Razak KA. 2012. Minocycline treatment reverses ultrasonic vocalization production deficit in a mouse model of Fragile X Syndrome. Brain Research 1439:7-14. doi: 10.1016/ j.brainres.2011.12.041.
71. Sales GD, Pye D. 1974. Ultrasonic communication by animals. London: Springer Netherlands.
72. Scattoni ML, McFarlane HG, Zhodzishsky V, Caldwell HK, Young WS, Ricceri L, Crawley JN. 2008. Reduced ultrasonic vocalizations in vasopressin 1b knockout mice. Behavioural Brain Research 187:371-378. doi: 10.1016/ j.bbr.2007.09.034.
73. Sewell GDS. 1972. Ultrasound and mating behaviour in rodents with some observations on other behavioural situations. Journal of Zoology 168:149-164. doi: 10.1111/j.1469-7998.1972.tb01345.x.
74. Shemesh Y, Sztainberg Y, Forkosh O, Shlapobersky T, Chen A, Schneidman E. 2013. High-order social interactions in groups of mice. eLife 2:e00759. doi: 10.7554/eLife.00759.
75. Shen JX, Feng AS, Xu ZM, Yu ZL, Arch VS, Yu XJ, Narins PM. 2008. Ultrasonic frogs show hyperacute phonotaxis to female courtship calls. Nature 453:914-916. doi: 10.1038/nature06719.
76. Shen SF, Akcay E, Rubenstein DR. 2014. Group size and social conflict in complex societies. The American Naturalist 183:301-310. doi: 10.1086/674378.
77. Silk JB. 2007. The adaptive value of sociality in mammalian groups. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 362:539-559. doi: 10.1098/rstb.2006.1994.
78. Sugimoto H, Okabe S, Kato M, Koshida N, Shiroishi T, Mogi K, Kikusui T, Koide T. 2011. A role for strain differences in waveforms of ultrasonic vocalizations during male-female interaction. PLOS ONE 6:e22093. doi: 10.1371/journal.pone.0022093.
79. Szykman M, Van Horn RC, Engh AL, Boydston EE, Holekamp KE. 2007. Courtship and mating in free-living spotted hyenas. Behaviour 144:815-846. doi: 10.1163/156853907781476418.
80. Thomas DA, Barfield RJ. 1985. Ultrasonic vocalization of the female rat (Rattus norvegicus) during mating. Animal Behaviour 33:720-725. doi: 10.1016/S0003-3472(85)80002-6.
81. 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 the United States of America 95: 1870-1875. doi: 10.1073/pnas.95.4.1870.
82. Van Oortmerssen GA. 1971. Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). A behaviour genetic study. Behaviour 38:1-92. doi: 10.1163/156853971X00014.
83. Warburton VL, Sales GD, Milligan SR. 1989. The emission and elicitation of mouse ultrasonic vocalizations: the effects of age, sex and gonadal status. Physiology & Behavior 45:41-47. doi: 10.1016/0031-9384(89)90164-9.
84. Weissbrod A, Shapiro A, Vasserman G, Edry L, Dayan M, Yitzhaky A, Hertzberg L, Feinerman O, Kimchi T. 2013. Automated long-term tracking and social behavioural phenotyping of animal colonies within a semi-natural environment. Nature Communications 4:2018. doi: 10.1038/ncomms3018.
85. White NR, Prasad M, Barfield RJ, Nyby JG. 1998. 40- and 70-kHz vocalizations of mice (Mus musculus) during copulation. Physiology & Behavior 63:467-473. doi: 10.1016/S0031-9384(97)00484-8.
86. Whitney G, Coble JR, Stockton MD, Tilson EF. 1973. Ultrasonic emissions: do they facilitate courtship of mice. Journal of Comparative and Physiological Psychology 84:445-452. doi: 10.1037/h0034899.
87. Zhang C, Florencio D, Ba DE, Zhang Z. 2008. Maximum likelihood sound source localization and beamforming for directional microphone arrays in distributed meetings. IEEE Transactions on Multimedia 10:538-548. doi: 10. 1109/TMM.2008.917406.