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Short Research Description
Social communication in Xenopus: development, function and evolution of neural circuits for producing and responding to vocal signals.
Full Research Description
Office under renovation: 913 Fairchild
Lab location: 914 Fairchild
Social communication is ubiquitous in animals; even the most solitary species meet to mate. Dedicated sensory, neural and muscular systems support social communication and determining how these systems work illuminates how one brain communicates with another.
Our goal is to determine how the nervous system produces and responds to social signals and to identify – across evolutionary timescales – the genetic changes that support the emergence of species differences in courtship communication. We study vocal communication specifically because this form of behavioral is readily described - and differences quantified - using acoustic analyses of sounds. We study African clawed frogs, Xenopus, because their social communication is dominated by vocal signaling. Females sing to males, males to females and to other males and these signals are specific to the sex of the signaler, the recipient and the social context. The genus – derived from terrestrial ancestors – is now entirely aquatic and includes 29 described species; each can be identified by specific, heritable features of male advertisement calls. Females are most sensitive to the acoustic features of male vocal signals from their own species.
The return to water from land in ancestral Xenopus, was accompanied by a novel means of vocal production still using the larynx but not requiring airflow and vocal cords. The male larynx is tuned to produce spectral features that contribute to unique vocal signatures of each species. The pattern of sound pulses that distinguish different species is produced by a specific neural circuit in the hindbrain., an ancient exaptation of hindbrain breathing circuits shared by all terrestrial vertebrates, including humans. Differences in vocal patterns between species have been mapped to key components of this hindbrain circuit.
Our current research aims to identify genomic loci associated with species specific vocal pattern production and perception using a genome-wide association approach and inter-fertile hybrids between relatively recently diverged Xenopus species: laevis, petersii, victorianus and poweri.
Barkan, C.L , Kelley, D.B. and Zornik, E. 2018. Premotor neuron evolution reflects divergent vocal behaviors, Journal of Neuroscience, 38, 5325-5337; doi: 10.1523/JNEUROSCI.0089-18.2018 pdf
Read reviews of this work in Nature, Science, and Journal of Neuroscience.
Barkan, C.L., Zornik, E. and Kelley, D.B. 2017. Evolution of vocal patterns: retuning hindbrain circuits during species divergence. Journal of Experimental Biology. 220: 856-867; doi: 10.1242/jeb.146845 pdf
Kelley, D.B., Elliott, T.M., Evans, B.J., Hall, I.C., Leininger. E.C., Rhodes, H.J., Yamaguchi, A. and Zornik.E. 2017. Probing forebrain to hindbrain circuit functions in Xenopus. Genesis 55 doi 10.1002/dvg.22999 pdf
Zornik, E., and Kelley, D.B. 2016 Hormones and vocal systems: Insights from Xenopus. In Hormones, Brain and Behavior Ed.3, D.W. Pfaff and M. Joels, Eds. Volume II, J. Balthazart, Ed. pdf
Hall, I.C., Kwong-Brown, U., Woolley, S.M.N and Kelley, D.B. 2016. Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus). J. Comp. Physiol. A, 202, 17-34. DOI 10.1007/s00359-015-1049-9 pdf
Evans BJ, Carter TF, Greenbaum E, Gvoždík V, Kelley DB, McLaughlin PJ, et al. (2015) Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa. PLoS ONE 10(12): e0142823. doi:10.1371/journal.pone.0142823. [pdf]
Albersheim-Carter, J., Blubaum, A., Ballagh, I., Missaghi, K., Siuda, E.R., McMurray, G., Bass, A.H., Dubuc, R., Kelley, D.B., Schmidt, M.F., Wilson, R. J.A., and Gray, P.A. 2015 Testing the evolutionary conservation of vocal motoneurons in vertebrates. Respiratory Physiology and Neurobiology. DOI: http://dx.doi.org/doi:10.1016/j.resp.2015.06.010
Leininger, E.C. and Kelley, D.B. 2015. Evolution of courtship songs in Xenopus; vocal pattern generation and sound production. Cytogenetic and Genome Research. DOI:10.1159/000433483
Leininger, E.C., Kitayama, K. and Kelley, D.B. 2015. Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus). Journal of Experimental Biology, 218, 849 - 857.
Tobias, M.L., Korsh, J. and Kelley, D.B. 2014. Evolution of male and female release calls in Xenopus, Behaviour, 148, 519 - 549.
Sweeney, L.S. and Kelley, D.B. 2014. Harnessing vocal patterns for social communication. Current Opinion in Neurobiology 28: 34 - 41.
Hall, I., Ballagh, I. and Kelley, D.B. 2013. The Xenopus amygdala mediates socially appropriate vocal communication signals. J. Neurosci. 33: 14543 - 14548.
Leininger, E.C. and Kelley, D.B. 2013. Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls. Proc. R. Soc. B, 7 April 280 no. 1756: 20122639
Nasipak, B.T. and Kelley, D.B. 2012. Developing laryngeal muscle of Xenopus laevis as a model system; androgen-driven myogenesis controls fiber type transformation. Devel. Neurobiol. 72, 664 - 675.
Tobias, M.L., Evans, B.J. and Kelley, D.B. 2011. Evolution of advertisement calls in African clawed frogs. Behaviour. In press. [pdf]
Zornik, E. and Kelley, D.B. 2011. Neuroendocrine basis for the hierarchical control of frog courtship vocalizations. Frontiers in Neuroendocrinology. In press. [pdf]
Elliott, T., Christensen-Dalsgaard, J., and Kelley, D. B. 2011. Temporally selective processing of communication signals by auditory midbrain neurons. J. Neurophysiol. 105: 1620 -1632. [pdf]
Tobias, M.L., Corke, A., Korsh, J., Yin, D., and Kelley, D. B. 2010. Vocal Competition in male Xenopus laevis frogs. Behav Ecol Sociobiol, 64(11): 1791 -1803. [pdf]
Kelley, D.B., and Bass, A.H. 2010. Neurobiology of vocal communication: mechanisms for sensorimotor integration and vocal patterning. Current Opinion in Neurobiology, 20, 748 -753. [pdf]
Evans, B.J., Greenbaum, E., Kusamba, C., Carter, T.F., Tobias, M.L., Mendel, S.A., and Kelley, D.B. 2010. Description of a new octoploid frog species (Anura: Pipidae: Xenopus from the Democratic Republic of the Congo, with a discussion of the biogeography of African clawed frogs in the Albertine Rift. J. Zoology. Epub. [pdf]
Evans, B.J., Tinsley, R., Carter, T., Tobias, M.L., and Kelley, D.B. 2008. A new species of clawed frog (genus Xenopus) from the Itombwe Plateau, Democratic Republic of the Congo: implications for DNA barcodes and biodiversity conservation. Zootaxa, 1780: 55-68. [pdf]
Yang, E.-J., and Kelley, D.B. 2008. Hormones and the regulation of vocal patterns in amphibians: Xenopus laevis vocalizations as a model system. In: Hormones, Brain and Behavior. D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach and R. Rubin (Eds), Academic Press, Vol. 2, 693 -705. [pdf]
Baur, L., Nasipak, B.T., and Kelley, D.B. 2008. Sexually differentiated, androgen-regulated, larynx-specific myosin heavy chain isoforms in Xenopus tropicalis and Xenopus laevis. Development, Genes, and Evolution. [pdf]
Nasipak, B.T. and Kelley, D.B. The genome of the diploid anuran Xenopus tropicalis contains a novel array of sarcoplasmic Myosin Heavy Chain genes expressed in larval muscle and larynx. Development, Genes, and Evolution. [pdf]
Zornik, E. and Kelley, D.B. 2008. Regulation of respiratory and vocal motor pools in the isolated brain of Xenopus laevis. J. Neurosci., 28: 612 - 621. [pdf]
Elliott, T.M., Christiansen-Dahlsgaard, J., and Kelley, D.B. 2007. Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis. J. Comp. Physiol. 93: 1243 - 1257. [pdf]
Yang, E.-J., Nasipak, B.T., and Kelley, D.B. 2007. Direct action of gonadotropin in brain integrates behavioral and reproductive functions. PNAS, 104:2477-2482. [pdf]
Elliott, T.M. and Kelley, D.B. 2007. Male discrimination of receptive and unreceptive female calls by temporal features. J. Exp. Biol. 210: 2836 - 2842. [pdf]
Zornik, E. and Kelley, D.B. 2007. Breathing and calling: neuronal networks in the Xenopus laevis hindbrain. J. Comp. Neurol., 501, 303 - 315. [pdf]
Vignal, C. and Kelley, D. B 2007. Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. Proc. R. Soc. B., 274, 479-488. [pdf]
Moore, F., Boyd, S., and Kelley, D.B. 2005. Historical perspective: hormonal regulation of behaviors in amphibians. Hormones and Behavior 28: 273 - 283. [pdf]
Evans, B.J., Kelley, D.B., Melnik, D.J., and Canatella, D.C. 2005. Evolution of RAG-1 in polyploid clawed frogs. Molecular Biology and Evolution, 22: 1193 - 1207.ÃÂ [pdf]
Kelley, D.B. 2004. Vocal communication in frogs. Current Opinion in Neurobiology, 14:751-757. [pdf]
Evans, B.J., Kelley, D.B., Tinsley, R.C., Melnick, D.J. and Canatella, D.C. 2004. A mitochondrial phylogeny of African clawed frogs: phylogeography and implications for polyploidy evolution. Molecular Phylogenetics and Evolution, 33, 197-213. [pdf]
Tobias, M.L., Barnard, C., O'Hagan, R., Horng, S., Rand, M. and Kelley, D.B. 2004. Vocal communication between male Xenopus laevis. Animal Behaviour, 67: 353-365. [pdf]
Yamaguchi, A., Kaczmarek, L., and Kelley, D.B. 2003. Functional specialization of male and female motoneurons. J. Neurosci. 23: 11568 - 11576 [pdf]
Wu, K.H., Tobias, M.T., and Kelley, D.B. 2003. Estrogen receptor expression in laryngeal muscle in relation to extrogen dependent increases in synaptic strength. Neuroendocrinology 78: 72-80. [pdf]
Wu, K.H., Tobias, M.T., Thornton, J.W. and Kelley, D.B. 2003. Estrogen receptors in Xenopus: Duplicate genes, splice variants, and tissue-specific expression. Gen. Comp. Endocrinol. 133: 38- 49 [pdf]
Brahic, C.J., and Kelley, D.B. 2003. Vocal circuitry in Xenopus laevis: telencephalon to laryngeal motor neurons. J. Comp. Neurol. 464: 115 - 130. [pdf]
Yamaguchi, A. and Kelley, D.B. 2002. Hormonal mechanisms of acoustic communication. In Acoustic Communication, A. Megala-Simmons, A. Popper and R. Fay, Eds. Springer Verlag, New York . [pdf]
Kelley, D.B. 2002. Hormonal regulation of motor output in amphibians; Xenopus laevis vocalizations as a model system. In Hormones,Brain and Behavior, D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach and R. Rubin (Eds), Academic Press [pdf]
Kelley, D. B. and Tindall, D.W. 2002. Model systems for the study of androgen regulated gene expression in the central nervous system, In Hormones, Brain and Behavior, D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach and R. Rubin (Eds), Academic Press. [pdf]
Breedlove, M, Jordan , C. and D.B. Kelley 2002. What neuromuscular systems tell us about hormones and behavior. In: Hormones, Brain and Behavior, D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach and R. Rubin (Eds), Academic Press. [pdf]
Kelley, D.B. and Brenowitz, E. 2002. Hormonal influences on courtship behavior. In: Behavioral Endocrinology, 2nd Ed. Becker, J., Breedlove, S.M., Crews, D., and McCarthy, M. (Eds). MIT Press. 289-325.
Wu, K.H., Tobias, M.L. and Kelley, D.B. 2001. Estrogen and laryngeal synaptic strength in Xenopus laevis; opposite effects of acute and chronic exposures. Neuroendocrinology 486: 1 - 11. [pdf]
Kelley, D.B. 2001. Is song special? Neuron 31:508-10. [pdf]
Edwards, C. and Kelley, D.B. 2001. Auditory and lateral line inputs to the midbrain of an aquatic anuran: neuroanatomical studies in Xenopus laevis. J. Comp. Neurol., 438, 148 - 162. [pdf]
Kelley, D.B., Tobias, M.L. and Horng, S. 2001. Producing and perceiving frogs songs; dissecting the neural bases for vocal behaviors in Xenopus laevis. In Anuran Communication, M. Ryan (Ed), Smithsonian Institution Press, pp. 156 - 166. [pdf]
Yamaguchi A, Kaczmarek LK, Kelley, D.B. 2000. Intrinsic membrane properties of laryngeal motoneurons that control sexually differentiated vocal behavior in African clawed frogs, Xenopus laevis. Biol Bull 2000 199:175-6 [pdf]
Yamaguchi, A. and Kelley, D.B. 2000. Generating sexually differentiated vocal patterns: laryngeal nerve and EMG recordings from vocalizing male and female African clawed frogs (Xenopus laevis). J. Neurosci., 20: 1559 - 1567. [pdf]
Edwards, C.J., Yamamoto, K., Kikuyama, S. and Kelley, D.B. 1999. Prolactin opens the sensitive period for androgen regulation of a larynx-specific myosin heavy chain gene. J. Neurobiol., 41, 453 - 451. [pdf]
Kay, J.N, Hannigan, P. and Kelley, D.B. 1999. Trophic effects of androgen: Development and hormonal regulation of neuron number in a sexually dimorphic vocal motor nucleus. J. Neurobiol., 40, 375 - 385. [pdf]
Kelley, D.B. and Tobias, M.L. 1999 The vocal repertoire of Xenopus laevis. In The Design of Animal Communication, M. Hauser and M. Konishi, Eds., MIT Press, Cambridge, pp 9 - 35. [pdf]
Tobias, M., Tomasson, J. and Kelley, D.B. 1998. Attaining and maintaining strong vocal synapses in female Xenopus laevis, J. Neurobiol., 37, 441 -448. [pdf]
Tobias, M.L.,Viswanathan, S. and Kelley, D.B. 1998. Rapping, a female receptive call, initiates male/female duets in the South African clawed frog, Proc. Natl. Acad. Sci., 95:1870 - 1875. [pdf] [ABC News Article]
Evans, B.J., Morales, J.C., Picker, M.D., Melnick, D.J., and Kelley, D.B. 1998. Absence of extensive introgression between Xenopus gilli and Xenopus laevis laevis (Anura: Pipidae) in Southwestern Cape Province, South Africa. Copeia, 2:504-509.[pdf]
Evans, B., Morales, J., Picker, M., Kelley, D.B. and Melnick, D. (1996). Comparative molecular phylogeography of two Xenopus species, X. gilli and X. laevis, in the South-western Cape Province, South Africa, Molecular Ecology, 6:333-343. Abstract [pdf]
Perez, J., Cohen, M.A. and Kelley, D.B. (1996). Androgen receptor mRNA expression in Xenopus laevis; sexual dimorphism and regulation in the laryngeal motor nucleus. J. Neurobiol. 30:556-568. Abstract [pdf]
Kelley, D. (1996). Sexual differentiation in Xenopus laevis. The Biology of Xenopus. R. Tinsely and H. Kobel (Eds.), Oxford University Press, pp. 143-176. [pdf]
Catz, D., Fischer, L. and Kelley, D. (1995) Androgen regulation of a laryngeal-specific myosin heavy chain isoform whose expression is sexually differentiated. Developmental Biology 171:448-457Abstract [pdf]
Fischer, L.M., Catz, D.S. & Kelley, D.B (1995) Androgen-Directed Development of the Xenopus Laevis Larynx: Control of Androgen Receptor Expression and Tissue Differentiation. Dev. Biol.; 170:115-126 [pdf]
Kang, L., Marin, M. and Kelley , D. 1995. Androgen biosynthesis and secretion in developing Xenopus laevis, Gen. Comp. Endocrinol., 100, 293 - 307. [pdf]
Tobias, M. and Kelley, D.B. 1995. Sexual differentiation and endocrine regulation of the laryngeal synapse in Xenopus laevis, J. Neurobiol., 28, 515 - 526. [pdf]
Fischer, L., Catz, D. & Kelley, D. (1993) An androgen receptor mRNA isoform associated with hormone-induced cell proliferation. Proc Natl Acad Sci USA 90:8254-8. Abstract [pdf]
Watson JT, Robertson J, Sachdev U, Kelley DB Laryngeal muscle and motor neuron plasticity in Xenopus laevis: testicular masculinization of a developing neuromuscular system. J Neurobiol 1993 Dec;24(12):1615-1625. Abstract [pdf]
Catz, D.S., Fischer, L.M., Moschella, M.C., Tobias, M.L. & Kelley, D.B. (1992) Sexually dimorphic expression of a laryngeal-specific androgen-regulated myosin heavy chain gene during Xenopus laevis development. Dev. Biol. 154:366-76. Abstract [pdf]
Watson JT, Kelley DB Testicular masculinization of vocal behavior in juvenile female Xenopus laevis reveals sensitive periods for song duration, rate, and frequency spectra. J Comp Physiol [A] 1992 Oct;171(3):343-350 Abstract [pdf]
Fischer, L.M. & Kelley, D.B. (1991) Androgen receptor expression and sexual differentiation of effectors for courtship song in Xenopus Laevis. The Neurosciences; Vol. 3:469-480 [pdf]
He, W.W., Fischer, L.M., Sun, S., Bilhartz, D.L., Zhu, X.P., Young, C.Y., Kelley, D.B. & Tindall, D.J. (1990) Molecular cloning of androgen receptors from divergent species with a polymerase chain reaction technique: complete cDNA sequence of the mouse androgen receptor and isolation of androgen receptor cDNA probes from dog, guinea pig and clawed frog. Biochem. Biophys. Res. Commun. 171:697-704. Abstract [pdf]
Kelley DB, Hayes M Amphibian experimental systems: developmental neurobiology and behavioral endocrinology in the clawed frog, Xenopus laevis. J Exp Zool Suppl 1990;4:148-149 Abstract
Tobias, M.L. & Kelley, D.B. (1988) Electrophysiology and dye-coupling are sexually dimorphic characteristics of individual laryngeal muscle fibers in Xenopus laevis. J Neurosci 8:2422-9. Abstract [pdf]
Kelley DB, Fenstemaker S, Hannigan P, Shih S. Sex differences in the motor nucleus of cranial nerve IX-X in Xenopus laevis: a quantitative Golgi study. J Neurobiol 1988 Jul;19(5):413-429 Abstract [pdf]
Kelley DB, Bockman RS, Weintraub A Prostaglandin regulation of reproductive behaviors in female Xenopus laevis: sources and target sites. Adv Prostaglandin Thromboxane Leukot Res 1987;17B:1133-1135 Abstract
Simpson HB, Tobias ML, Kelley DB. Origin and identification of fibers in the cranial nerve IX-X complex of Xenopus laevis: Lucifer Yellow backfills in vitro. J Comp Neurol. 1986 Feb 22; 244(4): 430-444. Abstract [pdf]
Kelley DB. Female sex behaviors in the South African clawed frog, Xenopus laevis: gonadotropin-releasing, gonadotropic, and steroid hormones. Horm Behav. 1982 Jun; 16(2): 158-174. No abstract available. [pdf]
Kelley DB. Locations of androgen-concentrating cells in the brain of Xenopus laevis: autoradiography with 3H-dihydrotestosterone. J Comp Neurol. 1981 Jun 20; 199(2): 221-231. Abstract
Reingold SC, Sejnowski TJ, Gelperin A, Kelley DB. [3H]-2-deoxyglucose autoradiography in a molluscan nervous system. Brain Res. 1981 Mar 16; 208(2): 416-420. Abstract
Erulkar, S.D., Kelley, D.B., Jurman, M.E., Zelman, F.P., Schneider, G.T. & Krieger, N.R. (1981) Modulation of the neural control of the clasp reflex in male Xenopus laevis by androgens: a multidisciplinary study. Proc Natl Acad Sci USA 78:5876-5880. Abstract
Sejnowski TJ, Reingold SC, Kelley DB, Gelperin A Localization of[3H]-2-deoxyglucose in single molluscan neurones. Nature. 1980 Oct 2; 287(5781): 449-451. Abstract
Wetzel DM, Kelley DB, Campbell BA Central control of ultrasonic vocalizations in neonatal rats: I. Brain stem motor nuclei. J Comp Physiol Psychol. 1980 Aug; 94(4): 596-605. Abstract
Kelley DB, Nottebohm F Projections of a telencephalic auditory nucleus-field L-in the canary. J Comp Neurol. 1979 Feb 1; 183(3): 455-469. Abstract
Kelley DB, Lieberburg I, McEwen BS, Pfaff DW Autoradiographic and biochemical studies of steroid hormone-concentrating cells in the brain of Rana pipiens. Brain Res. 1978 Jan 27; 140(2): 287-305. Abstract [pdf]
Kelley DB, Pfaff DW Hormone effects on male sex behavior in adult South African clawed frogs, Xenopus laevis. Horm Behav. 1976 Jun; 7(2): 159-182. Abstract
Morrell JI, Kelley DB, Pfaff DW Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian, Xenopus laevis. II. Estradiol. J Comp Neurol. 1975 Nov 1; 164(1): 63-77. Abstract
Kelley DB, Morrell JI, Pfaff DW Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian, Xenopus laevis. I. Testosterone. J Comp Neurol. 1975 Nov 1; 164(1): 47-59. Abstract