Two pup vocalization types are genetically and functionally separable in deer mice

Abstract

Vocalization is a widespread vertebrate social behavior that is essential for fitness in the wild. While many vocal behaviors are highly conserved, heritable features of specific vocalization types can vary both within and between species, raising the questions of why and how some vocal behaviors evolve. Here, using new computational tools to automatically detect and cluster vocalizations into distinct acoustic categories, we compare pup isolation calls across neonatal development in eight taxa of deer mice (genus Peromyscus) and compare them to laboratory mice (C57Bl6/j strain) and free-living, wild house mice (Mus musculus musculus). Whereas both Peromyscus and Mus pups produce ultrasonic vocalizations (USVs), Peromyscus pups also produce a second call type with acoustic features, temporal rhythms, and developmental trajectories that are distinct from those of USVs. In deer mice, these tonal and low frequency "cries" are predominantly emitted in postnatal days one through nine, while USVs are primarily made after day nine. Using playback assays, we show that cries result in a more rapid approach by Peromyscus mothers than USVs, suggesting a role for cries in eliciting parental care early in neonatal development. Using genetic crosses between two sister species of deer mice exhibiting large, innate differences in the acoustic structure of cries and USVs, we find that variation in vocalization rate, duration, and pitch display different degrees of genetic dominance and that cry and USV features can be uncoupled in second-generation hybrids. Taken together, this work shows that vocal behavior can evolve quickly between closely related rodent species in which vocalization types, likely serving distinct functions in communication, are controlled by distinct genetic loci.