A sex difference in synaptic efficacy at the laryngeal neuromuscular junction of Xenopus laevis

Tobias, Martha L.; Kelley, Darcy B.; Ellisman, Mark H.

doi:10.1523/jneurosci.15-03-01660.1995

Cited by 31 publications

(28 citation statements)

References 37 publications

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“…A characteristic feature of Xenopus male calls is amplitude modulation of the rapid trill; the initial clicks are low amplitude and loudness increases progressively throughout the trill. Amplitude modulation relies on a sexually dimorphic feature of the laryngeal neuromuscular synapse: males have weaker synapses than females as a result of less transmitter release from the motor terminal (26,27). Males use facilitation of the weak laryngeal synapse to progressively increase the number of muscle fibers contracting during nerve activity (28); facilitation is accompanied by amplitude modulation during the fast trill of the male call.…”

Section: Discussionmentioning

confidence: 99%

Rapping, a female receptive call, initiates male–female duets in the South African clawed frog

Tobias

Viswanathan

Kelley

1998

Proc. Natl. Acad. Sci. U.S.A.

151

130

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Finding a sexually receptive partner of the opposite sex is a challenge; one solution is to advertise. That advertising is usually the province of males has shaped scenarios for sexual selection, especially the ardent active male courting the passive but choosy female. Herein we consider an unusual case in which constraints on reproduction may have led to fertility advertisement by female frogs. When oviposition is imminent, female South African clawed frogs swim to an advertising male and produce an aphrodisiac call, rapping, that stimulates both male vocalization and approach. Males respond to rapping with a distinctive answer call. The rapping-answer interaction thus forms a duet between partners of a receptive pair.In most vertebrates, perhaps due to the greater investment of females in gametes and offspring (1), it is the male that competes for receptive conspecific females (2, 3). Many males find mates by advertising; prominent examples are mating leks and the songs of birds and frogs. This simple solution works well when the responding female can be identified by the signaling male. However, if the signaling environment is noisy or if population density is high, it may be difficult for the signaler to distinguish the responder. Under these conditions, we might expect a reciprocal signaling system involving both sexes. Herein we present evidence for a system of auditory recognition-receptive duets-in the South African clawed frog.We have studied male-female courtship vocalizations in Xenopus laevis, a member of a large genus of totally aquatic frogs from southern Africa (4). Xenopus inhabit murky ponds and mating occurs at night so that few if any visual cues are available to identify potential mates. Instead, it is believed that Xenopus, like other frogs (5), relies on auditory cues to broadcast receptivity and location. At the time we began our studies, two courtship vocalizations had been examined in this species. The advertisement or mating call (6) given only by sexually receptive males (7) is loud and prolonged with distinct fast and slow trill phases (7,8). Sexually receptive females display positive phonotaxis to tapes of advertisement calling (8). Ticking (6), given by sexually unreceptive females (9), is a quiet, slow, and monotonous trill (10) believed to function as a release call (6, 11).It has been assumed that male Xenopus find females by producing prolonged bouts of advertisement calling to which females are attracted; the male then clasps the nearest moving animal, releasing those that tick (12). The natural breeding conditions for Xenopus, high population density and low visibility, suggest that finding a mate may not be this simple. Unless the calling male could isolate himself from the rest of the group, clasping every animal in his vicinity would be disadvantageous; how then does he discriminate a responder?We have examined populations of Xenopus near Cape Town during the prolonged breeding season (about 6 months). Most (88%) adult males taken from these ponds were sexually rec...

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Section: Discussionmentioning

confidence: 99%

Rapping, a female receptive call, initiates male–female duets in the South African clawed frog

Tobias

Viswanathan

Kelley

1998

Proc. Natl. Acad. Sci. U.S.A.

151

130

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“…However sex differences do not exist in all cases. For example, the length of presynaptic active zones and the density of channels within them are not sexually dimorphic at the larynx of the African clawed frog (Tobias et al, 1995). Additionally, NMJ size (measured by acetylcholinesterase histochemistry) is not sexually dimorphic in a sonic muscle used for courtship in the oyster toadfish (Hirsch et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Sexual dimorphism in neuromuscular junction size on a muscle used in courtship by green anole lizards

O'Bryant

Wade

2001

J. Neurobiol.

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The green anole lizard exhibits seasonal courtship behavior that is sexually dimorphic. This courtship consists of the extension of a bright red throat fan (dewlap) associated with head-bobbing display behavior. While males extend their dewlaps in aggressive encounters as well as in courtship, females use their considerably smaller dewlaps much less frequently and mainly in agonistic encounters. In parallel, a number of components of the neuromuscular system controlling dewlap extension are greater in males than in females during the breeding season, including dewlap motoneuron soma size and muscle fiber size and number. These features do not seem to change substantially in adulthood, despite a dramatic decline in dewlap use during the nonbreeding season. We explored the morphology of this neuromuscular system in more detail in the present experiment in males and females during both the breeding and nonbreeding seasons. Fiber and whole muscle length (approximately perpendicular to the fibers) were measured. Acetylcholinesterase histochemistry was used to visualize neuromuscular junctions (NMJs), and the surface area and density of NMJs were assessed for each animal. During the breeding season, NMJ size was larger in males than in females, but NMJ density along each fiber was equivalent between the sexes. In addition, whole muscle length and that of individual muscle fibers, was larger in males than in females. However, when corrected for body size, the sex difference in muscle fiber length disappeared. In the nonbreeding season, the sexual dimorphisms were maintained, suggesting that these features do not change substantially due to differences in circulating testosterone or a difference in use across seasons. Overall, these results are consistent with the idea that enhanced NMJ size is a relatively stable feature of the dewlap muscle in adulthood that either facilitates or is a consequence of using a larger muscle to extend a bigger dewlap in males compared to females.

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“…Male laryngeal muscle activity increases over the course of a stimulus train delivered to the laryngeal nerve, due to the short-term strengthening of the weak laryngeal synapse with use (potentiation) [Tobias et al, 1995]. In females, the synapse is strong and does not potentiate [Ruel et al, 1998].…”

Section: Vocal Mechanisms: Sex and Species Differencesmentioning

confidence: 99%

“…The sex difference in strength of the laryngeal synapse is due to gonadal estrogen [Tobias et al, 1995]. The estrogen receptor is expressed in laryngeal muscle but not in motor neurons, so developmental strengthening presumably reflects a retrograde signal from muscle to motor neuron [Wu et al, 2003].…”

Section: Sexual Differentiation Of the Vpg And The Larynxmentioning

confidence: 99%

Evolution of Courtship Songs in <b><i>Xenopus</i></b>: Vocal Pattern Generation and Sound Production

Leininger

Kelley

2015

Cytogenet Genome Res

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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.

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A sex difference in synaptic efficacy at the laryngeal neuromuscular junction of Xenopus laevis

Cited by 31 publications

References 37 publications

Rapping, a female receptive call, initiates male–female duets in the South African clawed frog

Rapping, a female receptive call, initiates male–female duets in the South African clawed frog

Sexual dimorphism in neuromuscular junction size on a muscle used in courtship by green anole lizards

Evolution of Courtship Songs in <b><i>Xenopus</i></b>: Vocal Pattern Generation and Sound Production

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