Learning in honeybees: from molecules to behaviour

Studies in a variety of organisms as diverse as molluscs, insects, birds and mammals have shown that memories can exist in a variety of temporal domains ranging from short-term memories in the range of minutes to long-term memories lasting a lifetime. While transient covalent modifications of proteins underlie short-term memory, the formation of long-term memory requires gene expression and protein synthesis. Different intracellular signalling cascades have been implicated in distinct aspects of learning and memory formation. Little is known however, about how learning in intact animals is related to the modulation of these signalling cascades and how this contributes to distinct neuronal and behavioural changes in vivo. Associative learning in the honeybee provides the opportunity to study processes of memory formation by analysing its progression through different phases, across levels of behaviour, neural circuits, and cellular signalling pathways. The findings reveal evidence that various cellular signalling pathways in the neuronal circuit of distinct brain areas play a role in different processes during learning and memory formation.     

Kompass im Kopf

Ant compass – how desert ants learn to navigate Successful spatial orientation is a daily challenge for many animals. Cataglyphis desert ants are famous for their navigational performances. They return to the nest after extensive foraging trips without any problems. How do ants take their navigational systems into operation? After conducting different tasks in the dark nest for several weeks, they become foragers under bright sun light. This transition requires both a drastic switch in behavior and neuronal changes in the brain. Experienced foragers mainly rely on visual cues. They use a celestial compass and landmark panoramas. For that reason, naïve ants perform stereotype learning walks to calibrate their compass systems and acquire information about the nest's surroundings. During their learning walks, the ants frequently look back to the nest entrance to learn the homing direction. For aligning their gazes, they use the earth's magnetic field as a compass reference. This magnetic compass in Cataglyphis ants was previously unknown.     

Dress Nicer = Know More? Young Children’s Knowledge Attribution and Selective Learning Based on How Others Dress

This research explored whether children judge the knowledge state of others and selectively learn novel information from them based on how they dress. The results indicated that 4- and 6-year-olds identified a formally dressed individual as more knowledgeable about new things in general than a casually dressed one (Study 1). Moreover, children displayed an overall preference to seek help from a formally dressed individual rather than a casually dressed one when learning about novel objects and animals (Study 2). These findings are discussed in relation to the halo effect, and may have important implications for child educators regarding how instructor dress might influence young students’ knowledge attribution and learning preferences.     

Social learning of fear and safety is determined by the demonstrator's racial group

Social learning offers an efficient route through which humans and other animals learn about potential dangers in the environment. Such learning inherently relies on the transmission of social information and should imply selectivity in what to learn from whom. Here, we conducted two observational learning experiments to assess how humans learn about danger and safety from members (‘demonstrators'') of an other social group than their own. We show that both fear and safety learning from a racial in-group demonstrator was more potent than learning from a racial out-group demonstrator.     

Community through Culture: From Insects to Whales

It has become increasingly clear that social learning and culture occur much more broadly, and in a wider variety of animal communities, than initially believed. Recent research has expanded the list to include insects, fishes, elephants, and cetaceans. Such diversity allows scientists to expand the scope of potential research questions, which can help form a more complete understanding of animal culture than any single species can provide on its own. It is crucial to understand how culture and social learning present in different communities, as well as what influences community structure and culture may have on one another, so that the results across these different studies may most effectively inform one another. This review presents an overview of social learning in species across a spectrum of community structures, providing the necessary infrastructure to allow a comparison of studies that will help move the field of animal culture forward.     

The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Social cognition in humans

We review a diversity of studies of human social interaction and highlight the importance of social signals. We also discuss recent findings from social cognitive neuroscience that explore the brain basis of the capacity for processing social signals. These signals enable us to learn about the world from others, to learn about other people, and to create a shared social world. Social signals can be processed automatically by the receiver and may be unconsciously emitted by the sender. These signals are non-verbal and are responsible for social learning in the first year of life. Social signals can also be processed consciously and this allows automatic processing to be modulated and overruled. Evidence for this higher-level social processing is abundant from about 18 months of age in humans, while evidence is sparse for non-human animals. We suggest that deliberate social signalling requires reflective awareness of ourselves and awareness of the effect of the signals on others. Similarly, the appropriate reception of such signals depends on the ability to take another person's point of view. This ability is critical to reputation management, as this depends on monitoring how our own actions are perceived by others. We speculate that the development of these high level social signalling systems goes hand in hand with the development of consciousness.     

Social learning in non-grouping animals

Social learning is widespread in the animal kingdom and is involved in behaviours from navigation and predator avoidance to mate choice and foraging. While social learning has been extensively studied in group-living species, this article presents a literature review demonstrating that social learning is also seen in a range of non-grouping animals, including arthropods, fishes and tetrapod groups, and in a variety of behavioural contexts. We should not be surprised by this pattern, since non-grouping animals are not necessarily non-social, and stand to benefit from attending to and responding to social information in the same ways that group-living species do. The article goes on to ask what non-grouping species can tell us about the evolution and development of social learning. First, while social learning may be based on the same cognitive processes as other kinds of learning, albeit with social stimuli, sensory organs and brain regions associated with detection and motivation to respond to social information may be under selection. Non-grouping species may provide useful comparison taxa in phylogenetic analyses investigating if and how the social environment drives selection on these input channels. Second, non-grouping species may be ideal candidates for exploring how ontogenetic experience of social cues shapes the development of social learning, allowing researchers to avoid some of the negative welfare implications associated with raising group-living animals under restricted social conditions. Finally, while non-grouping species may be capable of learning socially under experimental conditions, there is a need to consider how non-grouping restricts access to learning opportunities under natural conditions and whether this places a functional constraint on what non-grouping animals actually learn socially in the wild.     

Social learning of predators in the dark: understanding the role of visual,chemical and mechanical information

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.     

Increased diversity and concordant shifts in community structure of coral‐associated Symbiodiniaceae and bacteria subjected to chronic human disturbance

Both coral‐associated bacteria and endosymbiotic algae (Symbiodiniaceae spp.) are vitally important for the biological function of corals. Yet little is known about their co‐occurrence within corals, how their diversity varies across coral species, or how they are impacted by anthropogenic disturbances. Here, we sampled coral colonies (n = 472) from seven species, encompassing a range of life history traits, across a gradient of chronic human disturbance (n = 11 sites on Kiritimati [Christmas] atoll) in the central equatorial Pacific, and quantified the sequence assemblages and community structure of their associated Symbiodiniaceae and bacterial communities. Although Symbiodiniaceae alpha diversity did not vary with chronic human disturbance, disturbance was consistently associated with higher bacterial Shannon diversity and richness, with bacterial richness by sample almost doubling from sites with low to very high disturbance. Chronic disturbance was also associated with altered microbial beta diversity for Symbiodiniaceae and bacteria, including changes in community structure for both and increased variation (dispersion) of the Symbiodiniaceae communities. We also found concordance between Symbiodiniaceae and bacterial community structure, when all corals were considered together, and individually for two massive species, Hydnophora microconos and Porites lobata, implying that symbionts and bacteria respond similarly to human disturbance in these species. Finally, we found that the dominant Symbiodiniaceae ancestral lineage in a coral colony was associated with differential abundances of several distinct bacterial taxa. These results suggest that increased beta diversity of Symbiodiniaceae and bacterial communities may be a reliable indicator of stress in the coral microbiome, and that there may be concordant responses to chronic disturbance between these communities at the whole‐ecosystem scale.     

Polymerase chain reaction primers for microsatellite loci in the semi‐aquatic grasshopper,Cornops aquaticum

The semi‐aquatic grasshopper Cornops aquaticum is native to South America, with a distribution as far south as the Argentinian pampas and as far north as the Gulf of Mexico. This study reports the characterization of nine microsatellite loci for this species. To our knowledge, no molecular studies have been conducted on C. aquaticum, therefore, little is known about this species’ genetic diversity and how this relates to host specificity. These primers will allow further studies to elucidate the population history of C. aquaticum across both its native and introduced ranges.     

Learning,fast and slow

Animals can learn efficiently from a single experience and change their future behavior in response. However, in other instances, animals learn very slowly, requiring thousands of experiences. Here, I survey tasks involving fast and slow learning and consider some hypotheses for what differentiates the underlying neural mechanisms. It has been proposed that fast learning relies on neural representations that favor efficient Hebbian modification of synapses. These efficient representations may be encoded in the genome, resulting in a repertoire of fast learning that differs across species. Alternatively, the required neural representations may be acquired from experience through a slow process of unsupervised learning from the environment.     

The contribution of recombination to heterozygosity differs among plant evolutionary lineages and life-forms

Background  

Despite its role as a generator of haplotypic variation, little is known about how the rates of recombination evolve across taxa. Recombination is a very labile force, susceptible to evolutionary and life trait related processes, which have also been correlated with general levels of genetic diversity. For example, in plants, it has been shown that long-lived outcrossing taxa, such as trees, have higher heterozygosity (H _e) at SSRs and allozymes than selfing or annual species. However, some of these tree taxa have surprisingly low levels of nucleotide diversity at the DNA sequence level, which points to recombination as a potential generator of genetic diversity in these organisms. In this study, we examine how genome-wide and within-gene rates of recombination evolve across plant taxa, determine whether such rates are influenced by the life-form adopted by species, and evaluate if higher genome-wide rates of recombination translate into higher H _e values, especially in trees.     

Neurotensin and neurotensin receptor 1 mRNA expression in song‐control regions changes during development in male zebra finches

Learned vocalizations are important for communication in some vertebrate taxa. The neural circuitry for the learning and production of vocalizations is well known in songbirds, many of which learn songs initially during a critical period early in life. Dopamine is essential for motor learning, including song learning, and dopamine‐related measures change throughout development in song‐control regions such as HVC, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), Area X, and the robust nucleus of the arcopallium (RA). In mammals, the neuropeptide neurotensin strongly interacts with dopamine signaling. This study investigated a potential role for the neurotensin system in song learning by examining how neurotensin (Nts) and neurotensin receptor 1 (Ntsr1) expression change throughout development. Nts and Ntsr1 mRNA expression was analyzed in song‐control regions of male zebra finches in four stages of the song learning process: pre‐subsong (25 days posthatch; dph), subsong (45 dph), plastic song (60 dph), and crystallized song (130 dph). Nts expression in LMAN during the subsong stage was lower compared to other time points. Ntsr1 expression was highest in HVC, Area X, and RA during the pre‐subsong stage. Opposite and complementary expression patterns for the two genes in song nuclei and across the whole brain suggest distinct roles for regions that produce and receive Nts. The expression changes at crucial time points for song development are similar to changes observed in dopamine studies and suggest Nts may be involved in the process of vocal learning. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 671–686, 2018     

Are ants botanists? Ant associative learning of plant chemicals mediates foraging for carbohydrates

1. Although associative learning is widespread across animals, its ecological importance is difficult to assess because learning is rarely studied in the field, where informative cues are juxtaposed against complex backgrounds of uninformative noise. 2. Ants rely heavily on chemical cues for foraging and engage in many ecologically important interactions with plants. Nevertheless, little is known about the role of associative learning of plant chemicals in ant foraging for carbohydrates. 3. In a field setting, the present study investigated whether the distantly related ant species Formica podzolica (Formicinae subfamily) and Tapinoma sessile (Dolichoderinae subfamily) exhibited associative learning of the chemical cues from two co-occurring plant species that are taxonomically and chemically distinct (Asteraceae: Helianthella quinquenervis and Apiaceae: Ligusticum porteri). 4. For two consecutive summers, ants were trained to forage from artificial sugar-rich baits associated with the leaf chemicals from either H. quinquenervis or L. porteri for 24 h, after which a two-choice test was deployed to assess whether ants would be more likely to select baits associated with the same (versus different) plant chemicals on which they had been trained. 5. The present study demonstrates associative learning of chemicals from both plant species, and these effects were consistent between ant species and years; training increased bait occupancy from 42% on the untrained scent to 66% on the trained scent. These results indicate that associative odour-learning may be widespread across ants and serve as an important mechanism mediating ant selection of resources.     

Discrimination: from behaviour to brain

Discrimination is a skill needed by many organisms for survival: decisions about food, shelter, and mate selection all require the ability to distinguish among stimuli. This article reviews the how and why of discrimination and how researchers may exploit this natural skill in the laboratory to learn more about what features of stimuli animals use to discriminate. The paper then discusses the possible neurophysiological basis of discrimination and proposes a model, based on one of stimulus-association put forth by Beninger and Gerdjikov (2004) [Beninger, R.J., Gerdjikov, T.V., 2004. The role of signaling molecules in reward-related incentive learning. Neurotox. Res., 6, 91-104], to account for the role of dopamine in how an animal learns to discriminate rewarded from non-rewarded stimuli.     

Development of Microplitis croceipes as a biological sensor

Classical conditioning, a form of associative learning, was first described in the vertebrate literature by Pavlov, but has since been documented for a wide variety of insects. Our knowledge of associative learning by insects began with Karl vonFrisch explaining communication among honeybees, Apis mellifera L. (Hymenoptera: Apidae). Since then, the honey bee has provided us with much of what we understand about associative learning in insects and how we relate the theories of learning in vertebrates to insects. Fruit flies, moths, and parasitic wasps are just a few examples of other insects that have been documented with the ability to learn. A novel direction in research on this topic attempts to harness the ability of insects to learn for the development of biological sensors. Parasitic wasps, especially Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), have been conditioned to detect the odors associated with explosives, food toxins, and cadavers. Honeybees and moths have also been associatively conditioned to several volatiles of interest in forensics and national security. In some cases, handheld devices have been developed to harness the insects and observe conditioned behavioral responses to air samples in an attempt to detect target volatiles. Current research on the development of biological sensors with insects is focusing on factors that influence the learning and memory ability of arthropods as well as potential mathematical techniques for improving the interpretation of the behavioral responses to conditioned stimuli. Chemical detection devices using arthropod‐based sensing could be used in situations where trained canines cannot be used (such as toxic environments) or are unavailable, electronic devices are too expensive and/or not of sufficient sensitivity, and when conditioning to target chemicals must be done within minutes of detection. The purpose of this article is to provide a brief review of the development of M. croceipes as a model system for exploring associative learning for the development of biological sensors.     

Primate home range and GRIN2A, a receptor gene involved in neuronal plasticity: implications for the evolution of spatial memory

N -methyl- d -aspartate (NMDA) glutamate receptors play crucial roles in neuronal synaptic plasticity, learning and memory. However, as to whether different NMDA subunits are implicated in specific forms of memory is unclear. Moreover, nothing is known about the interspecific genetic variability of the GRIN2A subunit and how this variation can potentially explain evolutionary changes in behavioral phenotypes. Here, we used 28 primate GRIN2A sequences and various proxies of memory across primates to investigate the role of GRIN2A . Codon-specific sequence analysis on these sequences showed that GRIN2A in primates coevolved with a likely ecological proxy of spatial memory (relative home-range size) but not with other indices of non-spatial learning and memory such as social memory and social learning. Models based on gene averages failed to detect positive selection in primate branches with major changes in relative home-range size. This implies that accelerated evolution is concentrated in specific parts of the protein expressed by GRIN2A . Overall, our molecular evolution study, the first on GRIN2A , supports the notion that different NMDA subunits may play a role in specific forms of memory and that phenotypic diversity along with genetic evolution can be used to investigate the link between genes and behavior across evolutionary time.     

A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition

Long-term exercise is associated with improved performance on a variety of cognitive tasks including attention, executive function, and long-term memory. Remarkably, recent studies have shown that even a single bout of aerobic exercise can lead to immediate improvements in declarative learning and memory, but less is known about the effect of exercise on motor learning. Here we sought to determine the effect of a single bout of moderate intensity aerobic exercise on motor skill learning. In experiment 1, we investigated the effect of moderate aerobic exercise on motor acquisition. 24 young, healthy adults performed a motor learning task either immediately after 30 minutes of moderate intensity running, after running followed by a long rest period, or after slow walking. Motor skill was assessed via a speed-accuracy tradeoff function to determine how exercise might differentially affect two distinct components of motor learning performance: movement speed and accuracy. In experiment 2, we investigated both acquisition and retention of motor skill across multiple days of training. 20 additional participants performed either a bout of running or slow walking immediately before motor learning on three consecutive days, and only motor learning (no exercise) on a fourth day. We found that moderate intensity running led to an immediate improvement in motor acquisition for both a single session and on multiple sessions across subsequent days, but had no effect on between-day retention. This effect was driven by improved movement accuracy, as opposed to speed. However, the benefit of exercise was dependent upon motor learning occurring immediately after exercise–resting for a period of one hour after exercise diminished the effect. These results demonstrate that moderate intensity exercise can prime the nervous system for the acquisition of new motor skills, and suggest that similar exercise protocols may be effective in improving the outcomes of movement rehabilitation programs.     

Salmon‐derived nutrients drive diatom beta‐diversity patterns

1. Pacific salmon are a textbook example of migratory animals that transfer nutrients between ecosystems, but little is known about how salmon‐derived nutrients (SDN) affect the biodiversity of recipient freshwater ecosystems. We examined paleolimnological records from six Alaskan lakes to define how changes in SDN from sockeye salmon (Oncorhynchus nerka) influenced sedimentary diatom community structure and beta‐diversity among lakes and through time. 2. Using an isotopic mixing model, we showed that SDN loading could account for >80% of the lake total nitrogen budgets and strongly regulated diatom community composition. Spatial dissimilarity in diatom communities was positively related to differences in SDN among lakes (r² = 0.69, P < 0.01, n = 10). Likewise, temporal dissimilarity in diatom communities was positively related to differences in SDN in a sediment core with substantial variation in salmon spawner dynamics between 1700 and 1950 AD (r² = 0.34, P < 0.01, n = 19). Finally, beta‐diversity metrics quantifying temporal turnover within each lake’s sediment record were also positively related to the variance in SDN loading among lakes (r² = 0.88, P < 0.05, n = 5). Mean SDN was only negatively correlated to temporal diatom beta‐diversity. 3. Spatially subsidised systems often receive temporally variable resource inputs, and thus, it is not surprising that, unlike previous studies, we found that resource variability was the key driver of community composition and beta‐diversity. In habitats that receive strongly fluctuating external nutrient loads, environment heterogeneity may overweigh stochastic community processes. In addition, freshwater diatoms are characterised by great dispersal capabilities and short life cycles and therefore may be a more sensitive indicator for evaluating the role of resource variability than previously used model organisms. These results suggest that productivity–diversity relationship vary with the nature of nutrient loading and the life history of the community studied. 4. Overall, our study highlights that the transport of nutrients by sockeye salmon across ecosystem boundaries is a significant driver of algal community and biodiversity in nursery lakes, mainly through changing the magnitude of nutrient variation. As such, freshwater species diversity in regions like the U.S. Pacific Northwest may become impoverished where there have been long‐term declines in salmon populations and decreases in nutrient variability among lakes.