Locomotor play behavior evolves by random genetic drift but not as a correlated response to selective breeding for high voluntary wheel-running behavior

Locomotor play is vigorous and seemingly purposeless behavior, commonly observed in young mammals. It can be costly in terms of energy expenditure, increased injury risk, and predator exposure. The main hypothesized benefit of locomotor play is enhancement of neuromuscular development, with effects persisting into adulthood. We hypothesized that levels of locomotor play would have evolved as a correlated response to artificial selection for increased voluntary exercise behavior. We studied mice from 4 replicate lines bred for voluntary wheel running (High Runner or HR) at 6–8 weeks of age and four non-selected Control (C) lines. Mice were weaned at 21 days of age and play behavior was observed for generations 20 (22–24 days old), 68 (22–23 days old), and 93 (15 days old). We quantified locomotor play as (1) rapid, horizontally directed jerk-run sequences and (2) vertical "bouncing." We used focal sampling to continuously record behavior in cages containing 4–6 individuals during the first 2–3 h of the dark cycle. Observations were significantly repeatable between observers and days. A two-way, mixed-model simultaneously tested effects of linetype (HR vs. C), sex, and their interaction. Contrary to our hypothesis, HR and C lines did not differ in any generation, nor did we find sex differences. However, differences among the replicate HR lines and among the replicate C lines were detected, and may be attributed to the effects of random genetic drift (and possibly founder effects). Thus, play behavior did evolve in this selection experiment, but not as a correlated response to selection for voluntary exercise.