Climate-Related Variation in Spatial Memory and Hippocampal Morphology in Food-Caching Chickadees.

Abstract

Harsh environments may lead to increased demands on memory in animals that rely on memory for survival. We previously showed that winter severity is associated with non-experience-based differences in memory and the hippocampus over a large continental scale in food-caching black-capped chickadees (Poecile atricapillus). However, large climatic differences also occur along steep elevational gradients in montane environments over a small geographic scale. Here we demonstrate for the first time that large differences in memory and the hippocampus exist over extremely short distances (10km) along the elevation gradient. We discovered that food-caching mountain chickadees (P. gambeli) from the highest elevations in the Sierra Nevada Mountains exhibited significantly better spatial memory associated with larger hippocampi with almost twice the number of hippocampal neurons compared to individuals only 600m lower in elevation. We found similarly large differences in hippocampal neurogenesis rates as indicated by the total number of immature neurons. Our study therefore suggests that climate-related environmental differences can produce dramatic differences in memory and the hippocampus in animals within close proximity on small spatial scales and that currently observed trends in global climate may have significant effects on cognition and the brain. Additionally, we attempted to integrate a new metric for enhanced spatial memory by looking specifically at the morphology of the neuron. 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. We show that neuron soma size in the hippocampus, 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. Finally, 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 to the wild-sampled birds, suggesting that at least some variation in neuron soma size may be due to environment-related plasticity. Our data suggests 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.