Evolution and Genetics of Precocious Burrowing Behavior in Peromyscus Mice

Summary A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits [1]. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus . In P. polionotus , burrows were excavated as early as 17 days of age, whereas P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species— P. polionotus adults excavate long burrows with an escape tunnel, whereas P. maniculatus dig short, single-tunnel burrows [2–4]—were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, we reciprocally cross-fostered pups of both species. Fostering did not alter the characteristic burrowing behavior of either species, suggesting that these differences are genetic. In backcross hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated and that a P. polionotus allele linked to tunnel length variation in adults is also associated with precocious onset of burrowing in juveniles, suggesting that the same genetic region—either a single gene with pleiotropic effects or linked genes—influences distinct aspects of the same behavior at these two life stages. These results raise the possibility that genetic variants affect behavioral drive (i.e., motivation) to burrow and thereby affect both the developmental timing and adult expression of burrowing behavior.