Species-specific loss of sexual dimorphism in vocal effectors accompanies vocal simplification in African clawed frogs (Xenopus)

Abstract

Phylogenetic studies can reveal patterns of evolutionary change, including the gain or loss of elaborate courtship traits in males. Male African clawed frogs generally produce complex and rapid courtship vocalizations, whereas female calls are simple and slow. In a few species, however, male vocalizations are also simple and slow, suggesting loss of male-typical traits. Here, we explore features of the male vocal organ that could contribute to loss in two species with simple, slow male calls. In Xenopus boumbaensis, laryngeal morphology is more robust in males than in females. Larynges are larger, have a more complex cartilaginous morphology and contain more muscle fibers. Laryngeal muscle fibers are exclusively fasttwitch in males but are both fast-and slow-twitch in females. The laryngeal electromyogram, a measure of neuromuscular synaptic strength, shows greater potentiation in males than in females. Malespecific physiological features are shared with X. laevis, as well as with a species of the sister clade, Silurana tropicalis, and thus are likely ancestral. In X. borealis, certain aspects of laryngeal morphology and physiology are sexually monomorphic rather than dimorphic. In both sexes, laryngeal muscle fibers are of mixed-twitch type, which limits the production of muscle contractions at rapid intervals. Muscle activity potentiation and discrete tension transients resemble female rather than male X. boumbaensis. The demasculinization of these laryngeal features suggests an alteration in sensitivity to the gonadal hormones that are known to control the sexual differentiation of the larynx in other Xenopus and Silurana species.

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

“…No potentiation is required for muscle contraction. X. borealis laryngeal muscle contains a mix of fast-and slow-twitch fibers in both sexes [Leininger et al, 2015]. These neural and muscular features support production of sound pulses at slow, but not rapid, rates.…”

“…The rapid CAP doublets produced by the VPG are separated by longer intervals, accounting for the long IPIs in the actual call. Male laryngeal muscle fibers are of the fasttwitch type and, after initial potentiation, capable of following longer bursts of rapid stimuli [Leininger et al, 2015]. However, the X. boumbaensis VPG does not generate prolonged, rapid bursts of activity .…”

“…X. borealis vocal sex differences are reduced, as female and male release call IPIs do not differ significantly. Adapted from Leininger et al [2015].…”

“…Vocal dimorphism is extreme because females do not produce release calls. The male X. boumbaensis vocal repertoire has independently evolved to the simple click-type advertisement pattern and a slow male release call that are more similar to the distantly related species (X. borealis) than to those of its own closest relatives [Leininger and Kelley, 2013;Leininger et al, 2015].…”

“…Available electromyogram (EMG) data in X. borealis suggest a large population of strong laryngeal synapses in [Leininger et al, 2015]. The X. laevis laryngeal neuromuscular synapse is mostly strong in adult females but mostly weak in adult males.…”