Differential hippocampal gene expression is associated with climate‐related natural variation in memory and the hippocampus in food‐caching chickadees

Abstract

There is significant and often heritable variation in cognition and its underlying neural mechanisms, yet specific genetic contributions to such variation are not well characterized. Black-capped chickadees present a good model to investigate the genetic basis of cognition because they exhibit tremendous climate-related variation in memory, hippocampal morphology and neurogenesis rates throughout the North American continent, and these cognitive traits appear to have a heritable basis. We examined the hippocampal transcriptome profiles of laboratory-reared chickadees from the two most divergent populations to test whether differential gene expression in the hippocampus is associated with population differences in spatial memory, hippocampal morphology and adult hippocampal neurogenesis rates. Using high-resolution mRNA sequencing coupled to a de novo transcriptome assembly, we generated 23 295 consensus sequences, which predicted 16 206 protein sequences with 13 982 showing high similarity to known protein sequences or conserved hypothetical proteins in other species. Of these, we identified differential expression in nearly 380 genes, with 47 genes specifically linked to neurogenesis, apoptosis, synaptic function, and learning and memory processes. Many of the other differentially expressed genes, however, may be associated with other functions. Our study presents the first avian hippocampal transcriptome, and it is the first study identifying differential gene expression associated with natural variation in cognition and the hippocampus. Our results provide additional support to the hypothesis that population differences in memory, hippocampal morphology and neurogenesis in chickadees have likely resulted from natural selection that appears to act on memory and its underlying neural mechanisms.

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

“…In both species, chickadees from harsher environments showed greater food-caching propensity, better spatial learning and memory, and larger hippocampus, a brain region involved in spatial cognition, with significantly more and larger neurons compared to chickadees from milder environments [2]. Differences in spatial cognition among populations appear to have a heritable basis, as they persisted in a common garden experiment [15] and were associated with differential gene expression in the hippocampus of chickadees reared and maintained in the same controlled environment [18]. Direct evidence in mammals also suggests that spatial memory and hippocampus volume are heritable [e.g., 19] and therefore available for selection.…”

“…We, however, measured spatial learning and memory, which are well known to be involved in cache retrieval [2,6,7] and previously documented population differences in spatial learning and memory associated with variation in winter climate [2,9,10]. In addition, there is some evidence that spatial learning and memory ability is heritable [13,15,18,19].…”

Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges

“…Sherry, ), which is assumed to be crucial to survival (Gibson & Kamil, ). Population comparisons and common garden experiments have provided evidence that climate harshness during the winter is driving positively the evolution of spatial memory abilities in black‐capped chickadee populations living at northern altitudes compared with their southern counterparts (Pravosudov et al ., , ; Roth et al ., ). This example highlights the key importance of not only targeting an appropriate model species and cognitive trait, but also relevant populations, because the strength of the selective agent (here, winter harshness) would be expected to lead to differential evolutionary predictions depending on the population; indeed the relationship between spatial memory and survival would be expected to be much stronger in northern chickadee populations compared with those living at milder latitudes.…”

“…Spatial memory allows storing positional information about important objects, including food, mates, and predators. Spatial memory is likely to be a key target in future evolutionary ecological studies, because it is mainly associated with a well‐defined portion of the mammalian, fish and avian brain, the hippocampus (Colombo & Broadbent, ; Rodríguez et al ., ; Hartley et al ., ), which provides a credible neurobiological target for selection (Pravosudov et al ., ). Again, food‐hoarding birds have been used extensively in this context, for instance by allowing individuals to hoard food freely in a test room containing artificial trees and noting relocation errors after a defined retention interval (Sherry, ; but see related discussion by Brodin & Urhan, ).…”

Visual landmark‐directed scatter‐hoarding of Siberian chipmunks Tamias sibiricus

“…Moreover, grey squirrels (Sciurus carolinensis) are able to remember the individual locations of nuts they have buried (McQuade et al 1986;Jacobs & Liman 1991). The rapidly expanding body of literature has shown that spatial memory of caches is crucial for various scatter-hoarding animals to relocate the food they have buried (Vander Wall 1990;Clayton & Dickinson 1998;Pravosudov et al 2013;Bednekoff & Balda 2014).…”