I Smell a Mouse: Indirect Genetic Effects on Voluntary Wheel-Running Distance, Duration and Speed

Indirect genetic effects (IGEs; the heritable influence of one organism on a conspecific) can affect the evolutionary dynamics of complex traits, including behavior. Voluntary wheel running is an important model system in quantitative genetic studies of behavior, but the possibility of IGEs on wheel running and its components (time spent running and average running speed) has not been examined. Here, we analyze a dataset from a replicated selection experiment on wheel running (11,420 control and 26,575 selected mice measured over 78 generations) in which the standard measurement protocol allowed for the possibility of IGEs occurring through odors because mice were provided with clean cages attached to a clean wheel or a wheel previously occupied by another mouse for 6 days. Overall, mice ran less on previously occupied wheels than on clean wheels, and they ran significantly less when following a male than a female. Significant interactions indicated that the reduction in running was more pronounced for females than males and for mice from selected lines than control mice. Pedigree-based “animal model” analyses revealed significant IGEs for running distance (the trait under selection), with effect sizes considerably higher for the initial/exploratory phase (i.e., first two of six test days). Our results demonstrate that IGEs can occur in mice interacting through scent only, possibly because they attempt to avoid conspecifics.