Cody A. Freas

Variation in memory and the hippocampus across populations from different climates: a common garden approach.

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individuals experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captive-raised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.

Elevation-related differences in memory and the hippocampus in mountain chickadees, Poecile gambeli

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 geographical scale. Here, we demonstrate for the first time that large differences in memory and the hippocampus exist over extremely short distances (10 km) along the elevation gradient. We found that food-caching mountain chickadees (P. gambeli) from the highest elevations in the Sierra Nevada Mountains had significantly better spatial memory associated with larger hippocampi, with almost twice the number of hippocampal neurons, than individuals only 600 m 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.

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

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.

Elevation-related differences in novel environment exploration and social dominance in food-caching mountain chickadees

Harsh and unpredictable environments have been assumed to favor the evolution of better learning abilities in animals. At the same time, individual variation in learning abilities might be associated with variation in other correlated traits potentially forming a behavioral syndrome. We have previously reported significant elevation-related differences in spatial memory and the hippocampus in food-caching mountain chickadees. Here, we tested for elevation-related differences in novel environment exploration, neophobia, and social dominance—behavioral traits previously thought to correlate with individual variation in cognition, using different birds from the same elevations. Compared to low-elevation birds, high-elevation chickadees were slower at novel environment exploration, but there were no detectable differences in neophobia. High-elevation chickadees were also socially subordinate to low-elevation chickadees in pairwise interactions. Considering previously reported elevation-related differences in cognition and the brain, our results suggest, however indirectly, that elevation-related variation in spatial memory might be associated with differences in novel environment exploration and in ability to obtain a high social rank in winter social groups. Whether these behavioral traits represent a behavioral syndrome or whether climate might affect these traits independently, our results suggest that multiple differences between elevations might assist with elevation-related separation. High-elevation chickadees would likely experience higher mortality if they move to lower elevation due to their low social dominance status and low-elevation chickadees might experience higher mortality if they move to higher elevation due to reduced memory ability and lack of behavioral adaptations to colder climate.

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

Summary 1. 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. 2. 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 foodcaching 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. 3. 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. 4. 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.

Path integration, views, search, and matched filters: the contributions of Rüdiger Wehner to the study of orientation and navigation

Rüdiger Wehner’s work on insect orientation and navigation has influenced many scientists studying navigation, not only in ants and bees, but in other animals as well. We review the scientific legacy of six topics arising from Wehner’s work on navigation. The polarisation compass is a chapter with a lot of behavioural and neurobiological detail. It has influenced the study of polarisation vision in other systems, and led Wehner to formulate the concept of a matched filter. The matched filter has probably had earlier formulations, but Wehner’s paper on it has been much cited in studies on navigation and in other fields. The polarisation compass serves the task of path integration in insects. Work on path integration took off in the 1980s with work on desert ants and rodents. The use of terrestrial visual cues, landmarks or the panorama in view-based matching is another major theme of navigational research today. Search strategies were also well described in desert ants, and this line of research helped to launch theoretical and empirical developments in searching behaviour, now a lively area of research. Finally, robotic work has often drawn inspiration from work on insect navigation. We end with some discussion of current research directions.

Compass cues used by a nocturnal bull ant, Myrmecia midas

ABSTRACT Ants use both terrestrial landmarks and celestial cues to navigate to and from their nest location. These cues persist even as light levels drop during the twilight/night. Here, we determined the compass cues used by a nocturnal bull ant, Myrmecia midas, in which the majority of individuals begin foraging during the evening twilight period. Myrmecia midas foragers with vectors of ≤5 m when displaced to unfamiliar locations did not follow the home vector, but instead showed random heading directions. Foragers with larger home vectors (≥10 m) oriented towards the fictive nest, indicating a possible increase in cue strength with vector length. When the ants were displaced locally to create a conflict between the home direction indicated by the path integrator and terrestrial landmarks, foragers oriented using landmark information exclusively and ignored any accumulated home vector regardless of vector length. When the visual landmarks at the local displacement site were blocked, foragers were unable to orient to the nest direction and their heading directions were randomly distributed. Myrmecia midas ants typically nest at the base of the tree and some individuals forage on the same tree. Foragers collected on the nest tree during evening twilight were unable to orient towards the nest after small lateral displacements away from the nest. This suggests the possibility of high tree fidelity and an inability to extrapolate landmark compass cues from information collected on the tree and at the nest site to close displacement sites. Summary: The nocturnal bull ant, Myrmecia midas, uses multiple cues to navigate and appears to rely heavily on landmark information for navigation.

Polarized light use in the nocturnal bull ant, Myrmecia midas

Solitary foraging ants have a navigational toolkit, which includes the use of both terrestrial and celestial visual cues, allowing individuals to successfully pilot between food sources and their nest. One such celestial cue is the polarization pattern in the overhead sky. Here, we explore the use of polarized light during outbound and inbound journeys and with different home vectors in the nocturnal bull ant, Myrmecia midas. We tested foragers on both portions of the foraging trip by rotating the overhead polarization pattern by ±45°. Both outbound and inbound foragers responded to the polarized light change, but the extent to which they responded to the rotation varied. Outbound ants, both close to and further from the nest, compensated for the change in the overhead e-vector by about half of the manipulation, suggesting that outbound ants choose a compromise heading between the celestial and terrestrial compass cues. However, ants returning home compensated for the change in the e-vector by about half of the manipulation when the remaining home vector was short (1−2 m) and by more than half of the manipulation when the remaining vector was long (more than 4 m). We report these findings and discuss why weighting on polarization cues change in different contexts.

The View from the Trees: Nocturnal Bull Ants, Myrmecia midas, Use the Surrounding Panorama While Descending from Trees

Solitary foraging ants commonly use visual cues from their environment for navigation. Foragers are known to store visual scenes from the surrounding panorama for later guidance to known resources and to return successfully back to the nest. Several ant species travel not only on the ground, but also climb trees to locate resources. The navigational information that guides animals back home during their descent, while their body is perpendicular to the ground, is largely unknown. Here, we investigate in a nocturnal ant, Myrmecia midas, whether foragers travelling down a tree use visual information to return home. These ants establish nests at the base of a tree on which they forage and in addition, they also forage on nearby trees. We collected foragers and placed them on the trunk of the nest tree or a foraging tree in multiple compass directions. Regardless of the displacement location, upon release ants immediately moved to the side of the trunk facing the nest during their descent. When ants were released on non-foraging trees near the nest, displaced foragers again travelled around the tree to the side facing the nest. All the displaced foragers reached the correct side of the tree well before reaching the ground. However, when the terrestrial cues around the tree were blocked, foragers were unable to orient correctly, suggesting that the surrounding panorama is critical to successful orientation on the tree. Through analysis of panoramic pictures, we show that views acquired at the base of the foraging tree nest can provide reliable nest-ward orientation up to 1.75 m above the ground. We discuss, how animals descending from trees compare their current scene to a memorised scene and report on the similarities in visually guided behaviour while navigating on the ground and descending from trees.

Limits of vector calibration in the Australian desert ant, Melophorus bagoti

Desert ants that forage solitarily continually update their position relative to the nest through path integration. This is accomplished by combining information from their celestial compass and pedometer. The path integration system can adapt when memories of previous inbound routes do not coincide with the outbound route, through vector calibration. Here, we test the speed and limit of vector calibration in the desert ant Melophorus bagoti by creating directional conflicts between the inbound and outbound routes (45°, 90°, 135°, 180°). The homeward vector appears to calibrate rapidly after training with shifts occurring after three foraging trips, yet the limit of the vector’s plasticity appears to be a maximum of 45°. At 45° conflicts, the vector calibrates the full 45°, suggesting dominance of the previous inbound memories over the outbound cues of the current trip. Yet at larger directional conflicts, vector shifts after training diminish, with foragers in the 90° and 135° conditions showing smaller intermediate shifts between the inbound memories and the current outbound vector. When the conflict is at its maximum (180°), foragers show no calibration, suggesting the outbound vector is dominant. Panorama exposure during training appears to aid foragers orienting to the true nest, but this also appears limited to about a 45° shift and does not improve with training.