A mechanism for punctuating equilibria during mammalian vocal development

Evolution and development are typically characterized as the outcomes of gradual changes, but sometimes (states of equilibrium can be punctuated by sudden change. Here, we studied the early vocal development of three different mammals: common marmoset monkeys, Egyptian fruit bats, and humans. Consistent with the notion of punctuated equilibria, we found that all three species undergo at least one sudden transition in the acoustics of their developing vocalizations. To understand the mechanism, we modeled different developmental landscapes. We found that the transition was best described as a shift in the balance of two vocalization landscapes. We show that the natural dynamics of these two landscapes are consistent with the dynamics of energy expenditure and information transmission. By using them as constraints for each species, we predicted the differences in transition timing from immature to mature vocalizations. Using marmoset monkeys, we were able to manipulate both infant energy expenditure (vocalizing in an environment with lighter air) and information transmission (closed-loop contingent parental vocal playback). These experiments support the importance of energy and information in leading to punctuated equilibrium states of vocal development.Author summary: Species can sometimes evolve suddenly; their appearance is preceded and followed by long periods of stability. This process is known as “punctuated equilibrium”. Our data show that for three mammalian species—marmoset monkeys, fruit bats, and humans—early vocal development trajectories can also be characterized as different equilibrium states punctuated by sharp transitions; transitions indicate the advent of a new vocal behavior. To better understand the putative mechanism behind such transitions, we show that a balance model, in which variables trade-off in their importance over time, captured this change by accurately simulating the shape of the developmental trajectory and predicting the timing of the transition between immature and mature vocal states for all three species. Two variables—energy and information—were hypothesized to trade-off during development. We tested and found support for this hypothesis in analyses of two marmoset monkey experiments, one which manipulated energy metabolic costs and another which manipulated information transmission.