The Genetic Architecture of Neonatal Deer Mouse Cries Implicates the Cerebellum in the Temporal Control of an Infant Social Behavior

Abstract

Vocal communication is a conserved vertebrate social behavior that begins at birth with the cries of infants. These neonatal vocal signals vary across contexts to elicit parental care that matches infant needs, and across species to match species-specific ecologies and social systems. This natural variation presents an opportunity to identify proximate mechanisms supporting flexible neonatal vocal behaviors and their evolution. To this end, we recently described neonatal vocalizations in North American deer mice, a model system for behavioral evolution, and identified heritable interspecific differences in features of these vocalizations. Here, we examine one of these features, temporal structure, which in humans and rodents contains information about infant distress. We find that temporal features of neonatal deer mouse cries have diverged more across deer mouse species than spectral features, and that in a playback assay cry duration affects the ability of pup vocalizations to elicit parental approach. To test proximate mechanisms underlying natural variation in cry duration, we first focus on the cerebellar system, a conserved hindbrain region that contributes to the temporal structure of motor rhythms. We identify interspecies variation in the gross anatomy of the neonatal cerebellum and inferior olive and show that pharmacological perturbation of olivocerebellar function alters the temporal structure of neonatal cries in deer mice. Next, we use an interspecies cross to map the genetic architecture underlying neonatal cry duration in deer mice. We identify a single quantitative trait locus significantly associated with cry duration, as well as candidate genes in this locus that could plausibly underlie species differences in the temporal structure of infant crying. Among these candidates are genes that are differentially expressed between species, function in the developing cerebellum, and have been linked to the duration of neonatal vocal signals in house mice. Taken as a whole, this work identifies contributions of the cerebellar system to neonatal social behaviors and suggests testable neural and genetic hypotheses about the evolution of infant crying.