The relationship between reliance on food caching, spatial memory and the hippocampus – an intraspecific comparison

The proposed research will investigate whether environmental conditions that place higher demands on spatial memory and the hippocampus result in enhanced spatial memory and an enlarged hippocampus with more neurons and higher cell proliferation rates. I will use a comparative method and a common garden experiment to test a prediction that black-capped chickadees in northern populations have evolved enhanced spatial memory and an enlarged hippocampus with more neurons. First, I will compare hippocampal structure in black-capped chickadees from twelve populations along latitudinal gradient. Food-caching birds rely on their caches to survive winters and use spatial memory for successful cache recovery. Both theoretical and empirical studies suggest that energetically demanding ecological conditions should result in more intensive food caching. Theoretical models also suggest that more caching along with successful cache recovery should significantly increase probability of survival in birds specifically when environmental conditions are more energetically demanding and unpredictable like those in northern populations.  It is thus reasonable to predict that chickadees living in more northern environments should depend on caches more heavily because of harsher winter conditions (lower air temperature, snow cover, shorter day length, longer winter) and thus should experience higher demands for spatial memory than their more southern conspecifics.  I expect that individuals from northern populations have an enlarged hippocampus with more neurons and higher hippocampal cell proliferation rates compared to their southern conspecifics. Comparing individuals of the same species will allow me to avoid potential pitfalls typical of inter-specific comparisons because different species might have many other ecological differences influencing their memory (Pravosudov & Clayton 2002). There could be two potential underlying mechanisms for the differences in memory and the hippocampus between northern and southern populations: (1) these differences might have a genetic basis as a result of higher selection pressure on memory in northern birds and (2) these differences might have an environmental basis and northern birds might have better memory and larger hippocampus as a result of more extensive food-caching experience. I will perform a common garden experiment in which northern and southern black-capped chickadees will be collected from nests and hand-raised in identical laboratory conditions. All birds will be given identical food-caching experience and then tested on various spatial memory tasks during their first winter. After behavioral experiments, I will sacrifice all birds for the analyses of hippocampal formation (volume, total number of neurons and cell proliferation rates) and the rest of the brain (mass, total volume). This study will thus test two predictions from the adaptive specialization hypothesis: (1) individuals in northern populations should have a relatively larger hippocampus with more neurons and higher cell proliferation rates and (2) these differences between northern and southern populations have evolved as a result of higher selection pressure on memory and the hippocampus and thus they are inherited.

COMPARISON OF MULTIPLE POPULATIONS. To establish a pattern that northern environmental conditions result in enhanced memory and an enlarged hippocampus, it is crucial to compare multiple populations to ensure that the differences between northern and southern chickadees are indeed due to environmental conditions associated with latitudinal gradient (shorter days, more snow, lower air temperatures). Black-capped chickadees present the best model to test the prediction that northern individuals have relatively larger hippocampal volume with more neurons compared to more southern individuals using multiple populations because this species has the largest south-north distribution among all North American food-caching species.

Because individuals from northern and southern populations might differ in body and total brain size, it is important to measure body size (wing length, tarsus, body mass) and total brain volume and brain mass to control for when testing for differences in the hippocampus. Comparative studies have always used relative hippocampal volume controlled for the overall telencephalon size. If birds in the north are simply bigger with bigger brains, they might have larger absolute hippocampus but there is no reason to expect that they will have relatively larger hippocampus simply because these birds are larger. Whereas it is possible that factors other than reliance on food caches might have contributed to possible differences between southern and northern individuals in body size or total brain size, hippocampus is a brain structure specifically involved in memory processing and thus relative hippocampal size is likely to have been affected specifically by the factors impacting memory. Interestingly, in my preliminary study black-capped chickadees from Alaska were significantly smaller than their southern conspecifics and they had significantly smaller brain volume, but they had significantly larger absolute and relative hippocampal volume with more neurons compared to southern chickadees (Pravosudov & Clayton 2002).

COMMON GARDEN EXPERIMENT. Another serious weakness of the Pravosudov & Clayton (2002) study concerns the fact that it remains unknown whether differences in memory and the hippocampus between Alaskan and Colorado black-capped chickadees are experience or genetic based. The adaptive specialization hypothesis implies that predicted enhanced memory and enlarged hippocampus in northern populations are genetically based as a result of higher selection pressure for better memory in northern populations. An alternative hypothesis is that some specific memory-related experiences directly affect memory and the hippocampus and northern individuals might have enhanced memory and larger hippocampus simply as a result of more such experiences. To establish that predicted differences between northern and southern populations in memory and the hippocampus are genetically based it is crucial to ensure that individuals from these populations share identical experiences. A common garden experiment in which all individuals are reared in identical environment is a good way to test whether any possible population differences in memory and the hippocampus are genetically based. In this study I will perform a common garden experiment by hand-raising black-capped chickadees from Alaska and Colorado in identical laboratory conditions and then testing for any possible differences between them in spatial memory, hippocampal volume, and neuron number. This would be the first experiment to test whether environmental conditions providing high selection pressure on memory and the hippocampus might result in evolution of enhanced spatial memory and an enlarged hippocampus within the same species.