Untangling Elevation-Related Differences in the Hippocampus in Food-Caching Mountain Chickadees: The Effect of a Uniform Captive Environment

Abstract

Variation in environmental conditions associated with differential selection on spatial memory has been hypothesized to result in evolutionary changes in the morphology of the hippocampus, a brain region involved in spatial memory. At the same time, it is well known that the morphology of the hippocampus might also be directly affected by environmental conditions. Understanding the role of environment-based plasticity is therefore critical when investigating potential adaptive evolutionary changes in the hippocampus associated with environmental variation. We previously demonstrated large elevation-related variation in hippocampus morphology in mountain chickadees over an extremely small spatial scale. We hypothesized that this variation is related to differential selection pressures associated with differences in winter climate severity along an elevation gradient, which make different demands on spatial memory used for food cache retrieval. Here, we tested whether such variation is experience based, generated by potential differences in the environment, by comparing the hippocampus morphology of chickadees from different elevations maintained in a uniform captive environment in a laboratory with those sampled directly from the wild. In addition, we compared hippocampal neuron soma size in chickadees sampled directly from the wild with those maintained in laboratory conditions with restricted and unrestricted spatial memory use via manipulation of food-caching experiences to test whether memory use can affect neuron soma size. There were significant elevation-related differences in hippocampus volume and the total number of hippocampal neurons, but not in neuron soma size, in captive birds. Captive environmental conditions were associated with a large reduction in hippocampus volume and neuron soma size, but not in the total number of neurons or in neuron soma size in other telencephalic regions. Restriction of memory use while in laboratory conditions produced no significant effects on hippocampal neuron soma size. Overall our results showed that captivity has a strong effect on hippocampus volume, which could be due, at least partly, to a reduction in neuron soma size specifically in the hippocampus, but it did not override elevation-related differences in hippocampus volume or in the total number of hippocampal neurons. These data are consistent with the idea of the adaptive nature of the elevation-related differences associated with selection on spatial memory, while at the same time demonstrating additional environment-based plasticity in hippocampus volume, but not in neuron numbers. Our results, however, cannot rule out that the differences between elevations might still be driven by some developmental or early posthatching conditions/experiences.

Environmental Influences on Spatial Memory and the Hippocampus in Food-Caching Chickadees

“…2. In both species, laboratory conditions did not eliminate population differences in food caching rates, spatial memory performance, and some hippocampal properties (most notably the total number of neurons; Freas et al, 2012;Freas, Bingman, et al, 2013;Pravosudov & Clayton, 2002).…”

“…In both black-capped and mountain chickadees, hippocampal neuron soma size was significantly associated with winter climate severity, with birds in harsher environments having larger hippocampal neuron soma (Figure 4; Freas, Bingman, et al, 2013). Similar to the hippocampus volume, hippocampal neuron soma size appears highly plastic, and captivity resulted in significant soma size reduction in both black-capped and mountain chickadees (Figure 4; Freas, Bingman, et al, 2013;Freas, Roth, et al, 2013).…”

“…The follow-up studies Roth & Pravosudov, 2009) compared 10 populations of black-capped chickadees along the winter climate gradient, including the two populations previously compared in Pravosudov and Clayton (2002). These studies showed that independent of latitudinal differences in day length (shorter in northern populations), harsher winter climatic conditions were associated with larger hippocampus volume, higher total number and larger soma size of hippocampal neurons, larger total number of hippocampal glial cells, and higher neurogenesis rates (Figure 2; Chancellor, Roth, LaDage, & Pravosudov, 2011;Freas, Bingman, LaDage, & Pravosudov, 2013;Roth et al, 2011;Roth & Pravosudov, 2009).…”

“…Higher elevations are associated with significantly lower winter temperatures (likely requiring more food intake to meet higher energetic demands), longer winter period associated with limited natural (e.g., not cached) food supply (likely increasing reliance on food caches for overwinter survival), and significantly more snow cover (both on the ground and on trees) that likely limits access to some potential foraging substrates. Similarly to black-capped chickadees from different winter conditions, mountain chickadees from higher elevations in the Sierra Nevada had a stronger propensity to cache food, better spatial memory ability, larger hippocampus volume, higher total number and larger soma size of hippocampal neurons, and higher hippocampal neurogenesis rates (Figure 3; Freas et al, 2012;Freas, Bingman, et al, 2013;Freas, Roth, LaDage, & Pravosudov, 2013).…”

Environmental Influences on Spatial Memory and the Hippocampus in Food-Caching Chickadees

“…While it is extremely likely that captivity-associated stress is one of the drivers for such changes, it remains unclear how memory-related experiences might affect hippocampal neuron soma size. At least in captive birds collected as juveniles from the wild, manipulating the number of memory experiences failed to produce a detectable effect on hippocampal neuron soma size (Freas, Bingman, et al, 2013).…”