The Genetics of Burrowing Behavior in Peromyscus Mice in the Lab and the Field

Abstract

Striking variation in animal behavior has repeatedly evolved among closely-related species over short evolutionary timescales. However, the proximate and ultimate mechanisms that give rise to behavioral diversity remain poorly understood. Here, we leverage variation in burrow architecture among deer mice (genus Peromyscus), which ranges from short and simple to long and complex. First, we discover that complete, adult-like burrowing behavior emerges earlier in postnatal development in a complex-burrowing species. We then identify a genetic region associated with both precocious burrowing in juveniles and burrow length in adults. Second, we find that the complex-burrowing species digs cooperatively with both same- and opposite-sex partners. However, opposite-sex pairs are more socially cohesive and more likely to engage in simultaneous, coordinated digging, thereby producing longer burrows than same-sex pairs. Third, we design and implement a custom radio frequency identification (RFID) system to non-invasively monitor burrow use in the wild. We find that, in nature, mice frequent the burrows of close genetic relatives and may receive inclusive fitness benefits by maintaining a network of shared burrows. Last, we develop a novel phenotyping platform for the high-throughput quantification of multiple components of burrowing behavior. Using this video-recorded assay, we uncover variation in the temporal dynamics of burrow construction that contribute to interspecific variation in overall burrow structure. We then use a genetic cross between mice with divergent burrow architectures to test for associations between genotype and behavior. By isolating the particular components of burrowing behavior that explain the bulk of heritable variation between species, we can begin to describe the number and types of mutations required to produce, over evolutionary time, a complex behavior from a relatively simple ancestral form. Taken together, these studies clarify the developmental and genetic mechanisms of burrowing behavior in Peromyscus and characterize the social and ecological contexts in which burrowing behavior is expressed.