Natural Selection and Spatial Cognition in Wild Food-Caching Mountain Chickadees

Understanding how differences in cognition evolve is one of the critical goals in cognitive ecology [1-5]. In food-caching species that rely on memory to recover caches, enhanced spatial cognition has been hypothesized to evolve via natural selection [2, 6-8], but there has been no direct evidence of natural selection acting on spatial memory. Food-caching mountain chickadees living at harsher, higher elevations, with greater reliance on cached food have better spatial learning abilities and larger hippocampi containing more and larger neurons compared to birds from milder, lower elevations [9, 10]. Here, we tested for natural selection on spatial cognition in wild food-caching mountain chickadees at high elevations and documented the following: (1) compared to first-year juveniles, adults showed significantly better performance on two spatial cognitive tasks-spatial learning and memory and a consecutive reversal learning task; (2) cognitive performance in both spatial learning and reversal learning tasks was not significantly different between years in the same chickadees tested in their first year of life and after surviving to their second winter; and (3) cognitive performance in the spatial learning task was significantly better among the first-year juveniles that survived to their second winter compared to the subset of juveniles that did not survive. Taken together, our results provide evidence for natural selection on spatial cognition in a food-caching species living in harsh environments and suggest that natural selection associated with local environmental conditions might be generating intraspecific differences in cognitive abilities. VIDEO ABSTRACT.