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The extant species of African clawed frogs (Xenopus and Silurana) provide an opportunity to link the evolution of vocal characters to changes in the responsible cellular and molecular mechanisms. In this review, we integrate several robust lines of research: evolutionary trajectories of Xenopus vocalizations, cellular and circuit-level mechanisms of vocalization in selected Xenopus model species, and Xenopus evolutionary history and speciation mechanisms. Integrating recent findings allows us to generate and test specific hypotheses about the evolution of Xenopus vocal circuits. We propose that reduced vocal sex differences in some Xenopus species result from species-specific losses of sexually differentiated neural and neuromuscular features. Modification of sex-hormone-regulated developmental mechanisms is a strong candidate mechanism for reduced vocal sex differences.
Figure 1. The sex-specific vocal repertoire of X. laevis illustrated as oscillograms (sound intensity versus time). A Female ticking. B Female rapping. C Male advertisement calling. D Male answer calling. E Male amplectant calling. F Male growling. G Male chirping. Scale bars are 500 ms except for F and G (250 ms). Calls are made up of trains of sound pulses that form distinctive temporal patterns. The male advertisement and answer calls include fast and slow trill portions and are thus biphasic; other calls are monophasic. Advertisement and answer calls are intensity-modulated; other calls are not. Though shown here normalized to maximum pulse intensity for clarity, some calls are loud (advertisement calls and rapping, for example) and some are soft (ticking and amplectant calls). The male advertisement call is given when alone or in the presence of conspecifics of either sex. Other call types are context specific and depend on the sex and reproductive state of the partner (social context). Modified from Zornik and Kelley [2011].
Fig. 2. A Male advertisement call temporal patterns range in complexity from single sound pulses repeated at long intervals (click patterns) to temporally complex biphasic calls. B Mapping of advertisement calls onto the molecular phylogeny of the Xenopodinae reveals that advertisement call patterns are homoplasious. For example, burst-type calls occur in all branches of the phylogeny. A parsimony analysis suggests that the moderately complex burst-type advertisement call structure is ancestral. This figure is reproduced from Leininger and Kelley [2013].
Fig. 3. Advertisement and release calls from X. laevis, X. boumbaensis, and X. borealis illustrate diversity in vocal sex differences in call complexity and IPI. In X. laevis (top), male advertisement and release call IPIs exceed those of females, and male calls are more temporally complex than female calls. X. boumbaensis (middle) and X. borealis (bottom) have temporally simplified male advertisement calls, with long IPIs. X. boumbaensis vocal sex differences are extreme, because females do not produce release calls. X. borealis vocal sex differences are reduced, as female and male release call IPIs do not differ significantly. Adapted from Leininger et al. [2015].
Fig. 4. Ex vivo preparations of the isolated brain and larynx. A Laryngeal nerve activity recorded from the isolated male X. laevis brain matches the pattern of sound pulses of the biphasic advertisement call. An LFP wave in the premotor nucleus DTAM coincides with fictive fast trill. B The isolated vocal organ (larynx) produces sound pulses (recorded with a hydrophone) when the laryngeal nerves (n) are stimulated, the muscles (m) contract, and the arytenoid disks (d) separate.
Fig. 5. Physiological bases of advertisement call production in X. boumbaensis. On the left, the preparation is indicated. The upper panel illustrates the calls; the middle panels show recordings from the laryngeal nerve (arrowhead) as it exits the brain; the lower panel illustrates results of electrically stimulating the laryngeal nerve (1.) and recording sounds (3.) produced by movements of the arytenoid disks (2.). A Sound oscillogram of the male X. boumbaensis advertisement call. The call is a series of sound pulses repeated at long (>1 s) intervals. B Enlargement of a single sound pulse. C 5-HT-evoked laryngeal nerve recordings from the isolated X. boumbaensis brain reveal neural activity repeated at call intervals (compare to A). D Enlargement of one instance of neural activity in C. Nerve activity is composed of compound action potential doublets. E Single stimuli delivered to the laryngeal nerve rootlets are not sufficient to cause sound pulse production. F Doublet stimuli approximating the temporal parameters of the compound action potential doublets is sufficient to produce a single sound pulse. Adapted from Leininger and Kelley [2013].
Fig. 6. Physiological bases of advertisement call production in X. borealis. A Sound oscillogram of the male X. borealis advertisement call. The call is a series of sound pulses repeated at ∼450-ms intervals. B 5-HT-evoked laryngeal nerve recordings from the isolated X. borealis brain reveal neural activity repeated at intervals similar to advertisement call sound pulse intervals (compare to A). C In the isolated X. borealis male larynx, a single laryngeal nerve stimulation (1.) elicits a laryngeal electromyogram (2.), which causes one laryngeal muscle contraction (measured by tension recordings, 3.) resulting in a single sound pulse (4.). D A single CAP recorded from the laryngeal nerve in a male X. borealis brain. X. borealis male CAPs more closely resemble the asynchronous X. laevis female CAPs (E) than the highly synchronous X. laevis male CAPs (F). A-D Adapted from Leininger and Kelley [2013]. E, F Adapted from Yamaguchi and Kelley [2000].
Fig. 7. A suite of hormonally controlled sex differences in the X. laevis vocal circuit contributes to vocal sex differences [reviewed in Zornik and Kelley, 2011]. Some behavioral traits - for example, sound pulse rate - rely both on brain and laryngeal mechanisms. Sex differences masculinize or feminize from a default juvenile state, in response to either androgens (A) or estrogens (E). Losses of these mechanisms are candidates for vocal evolution in species with reduced vocal sex differences, such as X. borealis.
