Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls

Abstract

Independent or convergent evolution can underlie phenotypic similarity of derived behavioural characters. Determining the underlying neural and neuromuscular mechanisms sheds light on how these characters arose. One example of evolutionarily derived characters is a temporally simple advertisement call of male African clawed frogs (Xenopus) that arose at least twice independently from a more complex ancestral pattern. How did simplification occur in the vocal circuit? To distinguish shared from divergent mechanisms, we examined activity from the calling brain and vocal organ (larynx) in two species that independently evolved simplified calls. We find that each species uses distinct neural and neuromuscular strategies to produce the simplified calls. Isolated Xenopus borealis brains produce fictive vocal patterns that match temporal patterns of actual male calls; the larynx converts nerve activity faithfully into muscle contractions and single clicks. In contrast, fictive patterns from isolated Xenopus boumbaensis brains are short bursts of nerve activity; the isolated larynx requires stimulus bursts to produce a single click of sound. Thus, unlike X. borealis, the output of the X. boumbaensis hindbrain vocal pattern generator is an ancestral burst-type pattern, transformed by the larynx into single clicks. Temporally simple advertisement calls in genetically distant species of Xenopus have thus arisen independently via reconfigurations of central and peripheral vocal neuroeffectors.

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

“…Laryngeal EMG potentiation and synaptic strength: evolutionary and developmental hypotheses Muscle potentiation in male X. boumbaensis enables production of single, same intensity clicks in response to doublets of nerve compound action potentials (Leininger and Kelley, 2013). We show here that EMG potentiation is marked, suggesting a weak facilitating neuromuscular synapse.…”

“…We show here that EMG potentiation is marked, suggesting a weak facilitating neuromuscular synapse. The temporally simplified male advertisement call of this species has more likely evolved via modifications to the hindbrain vocal pattern generator (Leininger and Kelley, 2013), rather than by changes to the neuromuscular synapse, the properties of which appear similar to those of X. laevis. In X. borealis, EMG potentiation in both sexes resembles that produced by the strong laryngeal synapse of female X. laevis (Tobias and Kelley, 1987).…”

“…The X. borealis larynx produces muscle contractions and sound pulses in response to each stimulus in a train (Leininger and Kelley, 2013). Complete muscle relaxation following contraction is necessary to produce pulse trains; substantial maintained tension prevents the sound-producing discs from returning to their original positions before the next nerve impulse (Tobias and Kelley, 1987).…”

“…Timescales differ between advertisement and release calls: 1 s and 0.5 s, respectively. ATPase adenosine triphosphatase EMG electromyogram ISI inter-stimulus interval LM laryngeal myosin heavy chain isoform PI EMG potentiation index %tt percent transient tension EMG potentiation in male X. boumbaensis plays a different functional role: it enables the production of single sound pulses in response to doublets of nerve activity (Leininger and Kelley, 2013). Here, we examine the neuromuscular mechanisms responsible for vocal sex differences in two species with simple and slow advertisement calls: X. boumbaensis and X. borealis.…”

“…We used these preparations to determine the physiological mechanisms producing the independently evolved, simple and slow advertisement calls of male X. borealis and X. boumbaensis (Leininger and Kelley, 2013). These phylogenetically distant species use distinct central and peripheral mechanisms to generate a similar, derived advertisement call structure.…”