Summary
We examined effects of exogenous androgen (testosterone and dihydrotestosterone) on vocalizations of ovariectomized, adult female South African clawed frogs,Xenopus laevis. When paired with sexually active males, all ovariectomized females exhibited ticking, the unreceptive or ‘release’ call. Ticking consists of low amplitude, regularly spaced clicks with a mean interclick interval of 154 ms. When androgen-treated and paired with sexually active males, these ovariectomized females also exhibited an aberrant call (atypical ticking) in which click multiples replaced the single clicks of ticking. Mean ICI's for atypical ticking were 37 ms for click doublets and 22 ms for click quadruplets. Androgen treatment decreased the total time spent vocalizing (typical and atypical ticking) by ovariectomized females.
All androgen-treated females were then tested repeatedly with sexually receptive females in an attempt to elicit the male-typical vocalization, mate calling. Six of 17 females did not vocalize at all, even when gonadotropin injected. Eight females gave rapid (mean ICI, 36 ms) trains of clicks in an irregular temporal pattern (tick-like calls). Three females gave brief trills with alternating fast and slow components. Comparison of mate calllike vocalizations of androgen-treated females to mate calling of males reveals that calls in females are considerably shorter in duration (female: 0.32 min versus male: 45 min) and slower in tempo (ICI's; fast trill, female: 21 ms, male: 14 ms; slow trill, female: 36 ms, male: 28 ms). Incomplete masculinization of the vocal pattern of females by androgen treatment in adulthood may be due to developmental constraints on the modifiability of the neurons and muscles responsible for calling.
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Abbreviations
- C :
-
cholesterol
- DHT :
-
dihydrotestosterone
- HCG :
-
human chorionic gonadotropin
- IBI :
-
interburst interval
- ICI :
-
interclick interval
- ovx :
-
ovariectomized
- T :
-
testosterone
References
Erulkar SD, Kelley DB, Jurman ME, Zemlan F, Schneider GT, Krieger NR (1981) Modulation of the neural control of the clasp reflex in maleXenopus laevis by androgens: a multidisciplinary study. Proc Natl Acad Sci 78:5876–5880
Goy RW, McEwen B (1980) Sexual differentiation of the brain. MIT Press, Cambridge
Gray G, Sassoon D, Kelley D (1985) Sexual dimorphism of muscle fiber types in the larynx ofXenopus laevis. Soc Neurosci Abstr 11:212
Gurney M (1982) Behavioral correlates of sexual differentiation in the zebra finch song system. Brain Res 231:152–172
Gurney ME, Konishi M (1980) Hormone induced sexual differentiation of brain and behavior in zebra finches. Science 208:1380–1383
Hannigan P, Kelley DB (1981) Male and female laryngeal motor neurons inXenopus laevis. Soc Neurosci Abstr 7:269
Hannigan P, Kelley DB (1983) Androgen effects on sexually dimorphic vocal behavior and laryngeal motor neurons of adult femaleXenopus laevis. Soc Neurosci Abstr 9:1093
Kalk M (1960) Climate and breeding inXenopus laevis. S Afr J Med Sci 11:271–276
Kelley DB (1980) Auditory and vocal nuclei in the frog brain concentrate sex hormones. Science 207:553–555
Kelley DB (1981) Locations of androgen-concentrating cells in the brain ofXenopus laevis: autoradiography with 3Hdihydrotestosterone. J Comp Neurol 199:221–231
Kelley DB (1982) Female sex behaviors in the South African clawed frogXenopus laevis: gonadotropin-releasing, gonadotropic and steroid hormones. Horm Behav 16:158–174
Kelley DB, Fenstemaker SB (1983) Sexually dimorphic neurons of the vocal production nucleus inXenopus laevis: a quantitative study. Soc Neurosci Abstr 9:1094
Kelley DB, Pfaff DW (1976) Hormone effects on male sex behavior in adult South African clawed frogs,Xenopus laevis. Horm Behav 7:159–182
Kelley DB, Pfaff DW (1978) Generalizations from comparative studies on neuroanatomical and endocrine mechanisms of sexual behavior. In: Hutchinson JB (ed) Biological determinants of sexual behavior. John Wiley and Sons, Chichester, pp 225–254
Kelley DB, Morrell JI, Pfaff DW (1975) Autoradiographic localization of hormone-concentrating cells in the brain of an amphibianXenopus laevis. I. Testosterone. J Comp Neurol 164:47–62
Rabb GB (1973) Evolutionary aspects of the reproductive behavior of frogs. In: Vial J (ed) Evolutionary biology of the anurans. Univ of Missouri Press, Columbia, pp 214–227
Ridewood WG (1898) On the structure and development of the hyobranchial skeleton and larynx inXenopus andPipa; with remarks on the affinities of the aglossa. Linn Soc J Zool 26:53–127
Russell W (1954) Experimental studies of the reproductive behavior ofXenopus laevis. I. The control mechanisms for clasping and unclasping and the specificity of hormone action. Behavior 7:113–188
Sassoon D, Segil N, Kelley D (1983) Androgen induced proliferation in the larynx of juvenileXenopus laevis. Soc Neurosci Abstr 9:1093
Sassoon D, Segil N, Kelley D (1986) Androgen-induced myogenesis and chondrogenesis in the larynx ofXenopus laevis. Dev Biol 113:135–145
Schmidt RS (1974) Neural correlates of frog calling. Trigeminal tegmentum. J Comp Physiol 42:229–254
Segil N, Silverman L, Kelley D, Rainbow T (1983) Androgen binding in the laryngeal muscle ofXenopus laevis: sex differences and hormonal regulation. Soc Neurosci Abstr 9: 1093
Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York
Simpson HB, Tobias ML, Kelley DB (1986) Origin and identification of fibers in the cranial nerve IX–X complex ofXenopus laevis: Lucifer Yellow backfills in vitro. J Comp Neurol 244:430–444
Tobias M, Kelley DB (1985) Physiological characterization of the sexually dimorphic larynx inXenopus laevis. Soc Neurosci Abstr 11:496
Weintraub A, Kelley DB, Bockman R (1985) Prostaglandin E2 induces receptive behaviors in femaleXenopus laevis. Horm Behav 19:386–399
Wetzel DM, Kelley DB (1983) Androgen and gonadotropin effects on male mate calls in South African clawed frogs,Xenopus laevis. Horm Behav 17:388–404
Wetzel DM, Haerter U, Kelley DB (1985) A proposed neural pathway for vocalization in South African clawed frogs,Xenopus laevis. J Comp Physiol A 157:749–761
Yager D (1982) A novel mechanism for underwater sound production inXenopus borealis. Am Zool 122:887
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Hannigan, P., Kelley, D.B. Androgen-induced alterations in vocalizations of femaleXenopus laevis: modifiability and constraints. J. Comp. Physiol. 158, 517–527 (1986). https://doi.org/10.1007/BF00603797
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DOI: https://doi.org/10.1007/BF00603797