Complex relationships between climate and reproduction in a resident montane bird.

Animals use climate-related environmental cues to fine-tune breeding timing and investment to match peak food availability. In birds, spring temperature is a commonly documented cue used to initiate breeding, but with global climate change, organisms are experiencing both directional changes in ambient temperatures and extreme year-to-year precipitation fluctuations. Montane environments exhibit complex climate patterns where temperatures and precipitation change along elevational gradients, and where exacerbated annual variation in precipitation has resulted in extreme swings between heavy snow and drought. We used 10 years of data to investigate how annual variation in climatic conditions is associated with differences in breeding phenology and reproductive performance in resident mountain chickadees (Poecile gambeli) at two elevations in the northern Sierra Nevada mountains, USA. Variation in spring temperature was not associated with differences in breeding phenology across elevations in our system. Greater snow accumulation was associated with later breeding initiation at high, but not low, elevation. Brood size was reduced under drought, but only at low elevation. Our data suggest complex relationships between climate and avian reproduction and point to autumn climate as important for reproductive performance, likely via its effect on phenology and abundance of invertebrates.

Texas field crickets (Gryllus texensis) use visual cues to place learn but perform poorly when intra- and extra-maze cues conflict.

Central place foraging field crickets are an ideal system for studying the adaptive value of learning and memory, but more research is needed on ecologically relevant cognition in these invertebrates. Here, we test the visuospatial place learning of Texas field crickets (Gryllus texensis) in a radial arm maze. Our study expands previous work on G. texensis cognition for accuracy measures and extends our previous findings on females to both sexes. Additionally, our study examines whether crickets use intra- or extra-maze cues to locate a food reward using a maze rotation that puts the cues in conflict. We found that male and female crickets improved performance over trials when measured by accuracy variables but not latency variables. Thigmotaxis negatively impacted performance in both sexes. In a reward-absent trial, both male and female crickets demonstrated place memory. When intra- and extra-maze cues conflicted during a rotation trial, crickets' performance was not better than chance. Our rotation results suggest that crickets may experience reciprocal overshadowing of conflicting cues - a result most often seen in other taxa with conflicting multi-modal cues. We conclude that crickets do not rely solely on: (1) a single-cue association, (2) route-following, or (3) their own scent cues to navigate the maze. Instead, male and female Texas field crickets seem to learn the location of the reward using a combination of proximal and distal cues. The possibility to test large numbers of wild-caught or laboratory-reared individuals opens the door to future investigations on the evolutionary ecology of visuospatial learning in these invertebrates.

How general is cognitive ability in non-human animals? A meta-analytical and multi-level reanalysis approach.

General intelligence has been a topic of high interest for over a century. Traditionally, research on general intelligence was based on principal component analyses and other dimensionality reduction approaches. The advent of high-speed computing has provided alternative statistical tools that have been used to test predictions of human general intelligence. In comparison, research on general intelligence in non-human animals is in its infancy and still relies mostly on factor-analytical procedures. Here, we argue that dimensionality reduction, when incorrectly applied, can lead to spurious results and limit our understanding of ecological and evolutionary causes of variation in animal cognition. Using a meta-analytical approach, we show, based on 555 bivariate correlations, that the average correlation among cognitive abilities is low (r = 0.185; 95% CI: 0.087-0.287), suggesting relatively weak support for general intelligence in animals. We then use a case study with relatedness (genetic) data to demonstrate how analysing traits using mixed models, without dimensionality reduction, provides new insights into the structure of phenotypic variance among cognitive traits, and uncovers genetic associations that would be hidden otherwise. We hope this article will stimulate the use of alternative tools in the study of cognition and its evolution in animals.

Testing the greater male variability phenomenon: male mountain chickadees exhibit larger variation in reversal learning performance compared with females.

The greater male variability phenomenon predicts that males exhibit larger ranges of variation in cognitive performance compared with females; however, support for this pattern has come exclusively from studies of humans and lacks mechanistic explanation. Furthermore, the vast majority of the literature assessing sex differences in cognition is based on studies of humans and a few other mammals. In order to elucidate the underpinnings of cognitive variation and the potential for fitness consequences, we must investigate sex differences in cognition in non-mammalian systems as well. Here, we assess the performance of male and female food-caching birds on a spatial learning and memory task and a reversal spatial task to address whether there are sex differences in mean cognitive performance or in the range of variation in performance. For both tasks, male and female mean performance was similar across four years of testing; however, males did exhibit a wider range of variation in performance on the reversal spatial task compared with females. The implications for mate choice and sexual selection of cognitive abilities are discussed and future directions are suggested to aid in the understanding of sex-related cognitive variation.

Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition.

Understanding the evolution of inter and intraspecific variation in cognitive abilities is one of the main goals in cognitive ecology. In scatter-caching species, spatial memory is critical for the recovery of food caches and overwinter survival, but its effects on reproduction are less clear. Better spatial cognition may improve pre-breeding condition allowing for earlier reproduction. Alternatively, when mated to males with better spatial memory, females may be able to invest more in reproduction which may allow increased offspring survival and hence higher fitness. Using wild food-caching mountain chickadees, we found that when environmental conditions were favourable for breeding, females mated to males with better spatial cognition laid larger clutches and fledged larger broods than females mated to males with worse cognitive performance. Our results support the hypothesis that females may increase their reproductive investment to gain indirect, genetic benefits when mated to high-quality males with better spatial cognitive abilities.

Correction to: 'Fluctuations in annual climatic extremes are associated with reproductive variation in resident mountain chickadees'.

[This corrects the article DOI: 10.1098/rsos.171604.].

Fluctuations in annual climatic extremes are associated with reproductive variation in resident mountain chickadees.

Mounting evidence suggests that we are experiencing rapidly accelerating global climate change. Understanding how climate change may affect life is critical to identifying species and populations that are vulnerable. Most current research focuses on investigating how organisms may respond to gradual warming, but another effect of climate change is extreme annual variation in precipitation associated with alternations between drought and unusually heavy precipitation, like that exhibited in the western regions of North America. Understanding climate change effects on animal reproductive behaviour is especially important, because it directly impacts population persistence. Here, we present data on reproduction in nest-box breeding, resident mountain chickadees inhabiting high and low elevations in the Sierra Nevada across 5 years. These 5 years of data represent the full range of climatic variation from the largest drought in five centuries to one of the heaviest snow years on record. There were significant differences in most reproductive characteristics associated with variation in climate. Both climate extremes were negatively associated with reproductive success at high and low elevations, but low-elevation chickadees had worse reproductive success in the largest drought year while high-elevation chickadees had worse reproductive success in the heaviest snow year. Considering that the frequency of extreme climate swings between drought and snow is predicted to increase, such swings may have negative effects on chickadee populations across the entire elevation gradient, as climatic extremes should favour different adaptations. Alternatively, it is possible that climate fluctuations might favour preserving genetic variation allowing for higher resilience. It is too early to make specific predictions regarding how increased frequency of extreme climate fluctuation may impact chickadees; however, our data suggest that even the most common species may be susceptible.

What makes specialized food-caching mountain chickadees successful city slickers?

Anthropogenic environments are a dominant feature of the modern world; therefore, understanding which traits allow animals to succeed in these urban environments is especially important. Overall, generalist species are thought to be most successful in urban environments, with better general cognition and less neophobia as suggested critical traits. It is less clear, however, which traits would be favoured in urban environments in highly specialized species. Here, we compared highly specialized food-caching mountain chickadees living in an urban environment (Reno, NV, USA) with those living in their natural environment to investigate what makes this species successful in the city. Using a 'common garden' paradigm, we found that urban mountain chickadees tended to explore a novel environment faster and moved more frequently, were better at novel problem-solving, had better long-term spatial memory retention and had a larger telencephalon volume compared with forest chickadees. There were no significant differences between urban and forest chickadees in neophobia, food-caching rates, spatial memory acquisition, hippocampus volume, or the total number of hippocampal neurons. Our results partially support the idea that some traits associated with behavioural flexibility and innovation are associated with successful establishment in urban environments, but differences in long-term spatial memory retention suggest that even this trait specialized for food-caching may be advantageous. Our results highlight the importance of environmental context, species biology, and temporal aspects of invasion in understanding how urban environments are associated with behavioural and cognitive phenotypes and suggest that there is likely no one suite of traits that makes urban animals successful.

Absence of population structure across elevational gradients despite large phenotypic variation in mountain chickadees (Poecile gambeli).

Montane habitats are characterized by predictably rapid heterogeneity along elevational gradients and are useful for investigating the consequences of environmental heterogeneity for local adaptation and population genetic structure. Food-caching mountain chickadees inhabit a continuous elevation gradient in the Sierra Nevada, and birds living at harsher, high elevations have better spatial memory ability and exhibit differences in male song structure and female mate preference compared to birds inhabiting milder, low elevations. While high elevation birds breed, on average, two weeks later than low elevation birds, the extent of gene flow between elevations is unknown. Despite phenotypic variation and indirect evidence for local adaptation, population genetic analyses based on 18 073 single nucleotide polymorphisms across three transects of high and low elevation populations provided no evidence for genetic differentiation. Analyses based on individual genotypes revealed no patterns of clustering, pairwise estimates of genetic differentiation (FST, Nei's D) were very low, and AMOVA revealed no evidence for genetic variation structured by transect or by low and high elevation sites within transects. In addition, we found no consistent evidence for strong parallel allele frequency divergence between low and high elevation sites within the three transects. Large elevation-related phenotypic variation may be maintained by strong selection despite gene flow and future work should focus on the mechanisms underlying such variation.

Potential Mechanisms Driving Population Variation in Spatial Memory and the Hippocampus in Food-caching Chickadees.

Harsh environments and severe winters have been hypothesized to favor improvement of the cognitive abilities necessary for successful foraging. Geographic variation in winter climate, then, is likely associated with differences in selection pressures on cognitive ability, which could lead to evolutionary changes in cognition and its neural mechanisms, assuming that variation in these traits is heritable. Here, we focus on two species of food-caching chickadees (genus Poecile), which rely on stored food for survival over winter and require the use of spatial memory to recover their stores. These species also exhibit extensive climate-related population level variation in spatial memory and the hippocampus, including volume, the total number and size of neurons, and adults' rates of neurogenesis. Such variation could be driven by several mechanisms within the context of natural selection, including independent, population-specific selection (local adaptation), environment experience-based plasticity, developmental differences, and/or epigenetic differences. Extensive data on cognition, brain morphology, and behavior in multiple populations of these two species of chickadees along longitudinal, latitudinal, and elevational gradients in winter climate are most consistent with the hypothesis that natural selection drives the evolution of local adaptations associated with spatial memory differences among populations. Conversely, there is little support for the hypotheses that environment-induced plasticity or developmental differences are the main causes of population differences across climatic gradients. Available data on epigenetic modifications of memory ability are also inconsistent with the observed patterns of population variation, with birds living in more stressful and harsher environments having better spatial memory associated with a larger hippocampus and a larger number of hippocampal neurons. Overall, the existing data are most consistent with the hypothesis that highly predictable differences in winter climate drive the evolution and maintenance of differences among populations both in cognition and in the brain via local adaptations, at least in food-caching parids.

Chickadees with bigger brains have smaller digestive tracts: a multipopulation comparison.

The factors leading to the evolution of large brain size remain controversial. Brains are metabolically expensive and larger brains demand higher maintenance costs. The expensive-tissue hypothesis suggests that when selection favors larger brains, evolutionary changes in brain size can occur without an overall increase in energetic costs when brain size represents a trade-off with the size of other expensive tissues, such as the digestive tract. Still, support for this hypothesis is equivocal. We compared mean brain mass, digestive tract mass (stomach and gut) and heart mass in 9 populations of black-capped chickadees along a gradient of winter climate severity. Mean brain mass and telencephalon volume showed significant population variation with larger brains associated with harsher winter conditions. Mean population brain mass and telencephalon volume were also negatively related to both stomach and gut mass. Mean population heart mass, on the other hand, was not significantly associated with either mean brain mass or winter climate severity. Mean brain mass was negatively associated with body mass, with chickadees from harsher environments being smaller but having larger brains and smaller digestive tracts. Our results are consistent with the expensive-tissue hypothesis, and suggest that a harsher winter climate might favor larger brains, which might be associated with a reduction in size of the digestive tract. These findings could potentially be a result of population differences in the winter climate diet related to the perishability of more efficient invertebrate-based food caches.