Hippocampal neuron soma size is associated with population differences in winter climate severity in food-caching chickadees

Differential demands on cognitive ability may be expected to result in the evolution of cognition and associated changes in underlying neural mechanisms. While most comparative studies of cognition have focused on volumetric brain measurements, it remains unclear whether neuron morphology, which appears to be directly linked to cognitive functions, may be responsive to differential selection on cognitive ability. Food-caching birds rely on caches to survive winter and use spatial memory to recover previously stored food. Birds in more harsh winter climates have been hypothesized to be more dependent on cached food, and therefore, their winter survival may be expected to be more memory-dependent relative to their conspecifics from the milder winter climates. Here, we show that neuron soma size in the hippocampus, a brain region involved in memory function, exhibits significant population variation associated with different environmental pressures on spatial memory related to differences in winter climate harshness in two species of food-caching chickadees. Comparing ten populations of black-capped chickadees and three populations of mountain chickadees along a gradient of winter climate harshness, we found that birds from harsher environments had significantly larger hippocampal neuron soma sizes. Using chickadees from the two most divergent populations reared in a laboratory environment, we showed that these differences appear to be at least partly heritable as significant differences between these populations remained in birds sharing the same laboratory environment. At the same time, laboratory-reared birds had significantly smaller neuron soma size compared with the wild-sampled birds, suggesting that at least some variation in neuron soma size may be due to environment-related plasticity. Our data suggest that environment-related selection on memory may generate differences in neuron morphology, which appear to be controlled by some heritable mechanisms and likely underlie population differences in spatial memory.