Hybrid chickadees are deficient in learning and memory

Identifying the phenotypes underlying postzygotic reproductive isolation is crucial for fully understanding the evolution and maintenance of species. One potential postzygotic isolating barrier that has rarely been examined is learning and memory ability in hybrids. Learning and memory are important fitness‐related traits, especially in scatter‐hoarding species, where accurate retrieval of hoarded food is vital for winter survival. Here, we test the hypothesis that learning and memory ability can act as a postzygotic isolating barrier by comparing these traits among two scatter‐hoarding songbird species, black‐capped (Poecile atricapillus) and Carolina chickadees (Poecile carolinensis), and their naturally occurring hybrids. In an outdoor aviary setting, we find that hybrid chickadees perform significantly worse on an associative learning spatial task and are worse at solving a novel problem compared to both parental species. Deficiencies in learning and memory abilities could therefore contribute to postzygotic reproductive isolation between chickadee species. Given the importance of learning and memory for fitness, our results suggest that these traits may play an important, but as yet overlooked, role in postzygotic reproductive isolation.     

Guppies learn faster to discriminate between red and yellow than between two shapes

Animal species are expected to evolve specialised cognitive abilities to solve the tasks that are critical for their fitness. The literature contains several examples of specialised cognitive abilities, but few regard fish. The guppy, Poecilia reticulata, is a freshwater fish in which females choose their mates based on colouration, and orange‐coloured fruits are important diet enrichments for both sexes. For these reasons, we expect that this species has evolved enhanced learning abilities in colour discrimination compared to other types of discrimination. The comparison between studies in which guppies were tested for colour discrimination and studies in which guppies were tested for shape discrimination seems to support this hypothesis, but direct testing is still lacking. We experimentally compared the learning performance of guppies trained in a red–yellow colour discrimination learning task and that of guppies trained in a shape discrimination learning task using the same, automated conditioning procedure. Guppies trained in the colour discrimination showed greater learning performance, which provides support to the hypothesis that guppies possess enhanced colour discrimination abilities. Moreover, we found that male guppies performed better than females in both shape and colour discrimination learning.     

The 'ghosts' that pester studies on learning in mosquitoes: guidelines to chase them off

The identification of memory and learning in medically important mosquito species has been of epidemiological interest mainly because of the implications of learning on the pattern of contact between vectors and hosts. Empirical results either showing or suggesting the existence of cognitive abilities in mosquitoes have been reported in a number of experimental studies, mainly based on the observation of individual fidelity towards subsets of specific resources, such as hosts, resting sites or breeding sites. A closer inspection of the design of these experiments shows that, with the exception of recent studies providing stronger evidence of learning in the genus Culex (Diptera: Culicidae), methodological shortcomings still hinder the possibility of eliminating alternative interpretations for these findings, in some cases because the experiments were not specifically designed to identify the phenomenon, but mostly because of a lack of appropriate controls or replication. By highlighting these limitations, while acknowledging the practical difficulties that are inherent to the field, we aim to help expel from future research the 'ghosts' that still preclude the achievement of more definite conclusions about the prevalence of memory and learning in this group of insects.     

Does Sleep Play a Role in Memory Consolidation? A Comparative Test

Sleep is a pervasive characteristic of mammalian species, yet its purpose remains obscure. It is often proposed that ‘sleep is for the brain’, a view that is supported by experimental studies showing that sleep improves cognitive processes such as memory consolidation. Some comparative studies have also reported that mammalian sleep durations are higher among more encephalized species. However, no study has assessed the relationship between sleep and the brain structures that are implicated in specific cognitive processes across species. The hippocampus, neocortex and amygdala are important for memory consolidation and learning and are also in a highly actived state during sleep. We therefore investigated the evolutionary relationship between mammalian sleep and the size of these brain structures using phylogenetic comparative methods. We found that evolutionary increases in the size of the amygdala are associated with corresponding increases in NREM sleep durations. These results are consistent with the hypothesis that NREM sleep is functionally linked with specializations of the amygdala, including perhaps memory processing.     

Functional and evolutionary trade-offs co-occur between two consolidated memory phases in Drosophila melanogaster

Memory is a complex and dynamic process that is composed of different phases. Its evolution under natural selection probably depends on a balance between fitness benefits and costs. In Drosophila, two separate forms of consolidated memory phases can be generated experimentally: anaesthesia-resistant memory (ARM) and long-term memory (LTM). In recent years, several studies have focused on the differences between these long-lasting memory types and have found that, at the functional level, ARM and LTM are antagonistic. How this functional relationship will affect their evolutionary dynamics remains unknown. We selected for flies with either improved ARM or improved LTM over several generations, and found that flies selected specifically for improvement of one consolidated memory phase show reduced performance in the other memory phase. We also found that improved LTM was linked to decreased longevity in male flies but not in females. Conversely, males with improved ARM had increased longevity. We found no correlation between either improved ARM or LTM and other phenotypic traits. This is, to our knowledge, the first evidence of a symmetrical evolutionary trade-off between two memory phases for the same learning task. Such trade-offs may have an important impact on the evolution of cognitive capacities. On a neural level, these results support the hypothesis that mechanisms underlying these forms of consolidated memory are, to some degree, antagonistic.     

Long-term potentiation and memory

The discovery of long-term potentiation (LTP) transformed research on the neurobiology of learning and memory. This did not happen overnight, but the discovery of an experimentally demonstrable phenomenon reflecting activity-driven neuronal and synaptic plasticity changed discussions about what might underlie learning from speculation into something much more concrete. Equally, however, the relationship between the discovery of LTP and research on the neurobiology of learning and memory has been reciprocal; for it is also true that studies of the psychological, anatomical and neurochemical basis of memory provided a developing and critical intellectual context for the physiological discovery. The emerging concept of multiple memory systems, from 1970 onwards, paved the way for the development of new behavioural and cognitive tasks, including the watermaze described in this paper. The use of this task in turn provided key evidence that pharmacological interference with an LTP induction mechanism would also interfere with learning, a finding that was by no means a foregone conclusion. This reciprocal relationship between studies of LTP and the neurobiology of memory helped the physiological phenomenon to be recognized as a major discovery.     

Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions

Spatial cognition is predicted to be a fundamental component of fitness in many lizard species, and yet some studies suggest that it is relatively slow and inflexible. However, such claims are based on work conducted using experimental designs or in artificial contexts that may underestimate their cognitive abilities. We used a biologically realistic experimental procedure (using simulated predatory attacks) to study spatial learning and its flexibility in the lizard Eulamprus quoyii in semi-natural outdoor enclosures under similar conditions to those experienced by lizards in the wild. To evaluate the flexibility of spatial learning, we conducted a reversal spatial-learning task in which positive and negative reinforcements of learnt spatial stimuli were switched. Nineteen (32%) male lizards learnt both tasks within 10 days (spatial task mean: 8.16 ± 0.69 (s.e.) and reversal spatial task mean: 10.74 ± 0.98 (s.e.) trials). We demonstrate that E. quoyii are capable of flexible spatial learning and suggest that future studies focus on a range of lizard species which differ in phylogeny and/or ecology, using biologically relevant cognitive tasks, in an effort to bridge the cognitive divide between ecto- and endotherms.     

Memory,language, and ageing.

This overview provides both theoretical and empirical reasons for emphasizing practice and familiar skills as a practical strategy for enhancing cognitive functioning in old age. Our review of empirical research on age-related changes in memory and language reveals a consistent pattern of spared and impaired abilities in normal old age. Relatively preserved in old age is memory performance involving highly practised skills and familiar information, including factual, semantic and autobiographical information. Relatively impaired in old age is memory performance that requires the formation of new connections, for example, recall of recent autobiographical experiences, new facts or the source of newly acquired facts. This pattern of impaired new learning versus preserved old learning cuts across distinctions between semantic memory, episodic memory, explicit memory and perhaps also implicit memory. However, familiar verbal information is not completely preserved when accessed on the output side rather than the input side: aspects of language production, namely word finding and spelling, exhibit significant age-related declines. This emerging pattern of preserved and impaired abilities presents a fundamental challenge for theories of cognitive ageing, which must explain why some aspects of language and memory are more vulnerable to the effects of ageing than others. Information-universal theories, involving mechanisms such as general slowing that are independent of the type or structure of the information being processed, require additional mechanisms to account for this pattern of cognitive aging. Information-specific theories, where the type or structure of the postulated memory units can influence the effects of cognitive ageing, are able to account for this emerging pattern, but in some cases require further development to account for comprehensive cognitive changes such as general slowing.     

Spatial mapping memory: methods used to determine the existence and type of cognitive maps in arboreal mammals

1. Researchers have used multiple methods to understand spatial mapping memory used by arboreal mammals for orientation: the change-point test, measures of path tortuosity, field experiments with feeding platforms, nearest-neighbour feeding tree methods, complex calculations of travel route parameters, and theoretical models.
2. This literature review provides details of all of these methods, highlights previous results from spatial mapping memory studies, and discusses perspectives for future studies.
3. Previous studies have shown that various arboreal mammals, mostly in the order Primates, can memorise spatial environments using a cognitive map. Two types of maps are characterised: the topological map, based on landmarks and reused routes, and the Euclidean map, including the ability to create shortcuts by measuring distances and distinguishing between directions. Most of the studies showed that mammals do not travel randomly but, due to the difficulty of determining which spatial map is used, the use of cognitive maps remains hypothetical.
4. When studying spatial mapping memory, data collection and analysis should account for the species’ characteristics, such as the home-range size, food preferences, and types of movements. The role of sensory cues (visual, auditory, olfactory) is crucial to understanding spatial orientation. The most relevant way to determine how arboreal mammals orientate themselves in space is by using a mix of methods: random theoretical models, collecting data in a controlled environment, measuring different parameters of travel patterns, and considering the use of sensory cues and environmental factors of the study sites.
5. Research pertaining to spatial mapping memory in arboreal mammals and forest-dwelling mammals is important for understanding cognitive abilities in mammal species, and more studies are needed in mammals of various orders.

     

Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience

Although the neural and genetic pathways underlying learning and memory formation seem strikingly similar among species of distant animal phyla, several more subtle inter- and intraspecific differences become evident from studies on model organisms. The true significance of such variation can only be understood when integrating this with information on the ecological relevance. Here, we argue that parasitoid wasps provide an excellent opportunity for multi-disciplinary studies that integrate ultimate and proximate approaches. These insects display interspecific variation in learning rate and memory dynamics that reflects natural variation in a daunting foraging task that largely determines their fitness: finding the inconspicuous hosts to which they will assign their offspring to develop. We review bioassays used for oviposition learning, the ecological factors that are considered to underlie the observed differences in learning rate and memory dynamics, and the opportunities for convergence of ecology and neuroscience that are offered by using parasitoid wasps as model species. We advocate that variation in learning and memory traits has evolved to suit an insect's lifestyle within its ecological niche.     

Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.     

Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus

CRISPR-Cas is a form of adaptive sequence-specific immunity in microbes. This system offers unique opportunities for the study of coevolution between bacteria and their viral pathogens, bacteriophages. A full understanding of the coevolutionary dynamics of CRISPR-Cas requires knowing the magnitude of the cost of resisting infection. Here, using the gram-positive bacterium Streptococcus thermophilus and its associated virulent phage 2972, a well-established model system harbouring at least two type II functional CRISPR-Cas systems, we obtained different fitness measures based on growth assays in isolation or in pairwise competition. We measured the fitness cost associated with different components of this adaptive immune system: the cost of Cas protein expression, the constitutive cost of increasing immune memory through additional spacers, and the conditional costs of immunity during phage exposure. We found that Cas protein expression is particularly costly, as Cas-deficient mutants achieved higher competitive abilities than the wild-type strain with functional Cas proteins. Increasing immune memory by acquiring up to four phage-derived spacers was not associated with fitness costs. In addition, the activation of the CRISPR-Cas system during phage exposure induces significant but small fitness costs. Together these results suggest that the costs of the CRISPR-Cas system arise mainly due to the maintenance of the defence system. We discuss the implications of these results for the evolution of CRISPR-Cas-mediated immunity.     

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

Cognition is defined as the processes by which animals collect, retain and use information from their environment to guide their behaviour. Thus cognition is essential in a wide range of behaviours, including foraging, avoiding predators and mating. Despite this pivotal role, the evolutionary processes shaping variation in cognitive performance among individuals in wild populations remain very poorly understood. Selection experiments in captivity suggest that cognitive traits can have substantial heritability and can undergo rapid evolution. However only a handful of studies have attempted to explore how cognition influences life‐history variation and fitness in the wild, and direct evidence for the action of natural or sexual selection on cognition is still lacking, reasons for which are diverse. Here we review the current literature with a view to: (i) highlighting the key practical and conceptual challenges faced by the field; (ii) describing how to define and measure cognitive traits in natural populations, and suggesting which species, populations and cognitive traits might be examined to greatest effect; emphasis is placed on selecting traits that are linked to functional behaviour; (iii) discussing how to deal with confounding factors such as personality and motivation in field as well as captive studies; (iv) describing how to measure and interpret relationships between cognitive performance, functional behaviour and fitness, offering some suggestions as to when and what kind of selection might be predicted; and (v) showing how an evolutionary ecological framework, more generally, along with innovative technologies has the potential to revolutionise the study of cognition in the wild. We conclude that the evolutionary ecology of cognition in wild populations is a rapidly expanding interdisciplinary field providing many opportunities for advancing the understanding of how cognitive abilities have evolved.     

Ecological frames of mind: the role of cognition in behavioral ecology.

Cognitive psychology is the study of how information, from the senses and from memory, is used in the production of behavior. Investigation of the specifics of behavioral adaptation has already led some behavioral ecologists into the domain of animal cognition. I make several arguments for the benefits and the necessity of a sophisticated assessment by ecologists of the cognitive aspects of behavioral adaptation. First, because cognition typically serves to produce adaptive behavior, cognitive structure and function should reflect ecological demands; studies of cognition in ecological contexts are opportunities to understand adaptation. Furthermore, constraints on cognitive properties may help determine how behavior meets the environment. Studies of spatial memory in food-caching corvids exemplify how cognitive aspects of behavior may both reflect and determine specifics of adaptation. Second, many models in behavioral ecology assume certain cognitive abilities, such as timing or counting. Cognitive theory and methodology should be used to determine whether animals possess these abilities. I have provided examples. Third, consideration of cognitive function can lead to original ideas about the details of behavioral adaptation. Without a thorough integration of cognitive psychology with behavioral ecology, our understanding of the relation between behavior and selective pressures will be compromised.     

Evidence supporting the microbiota–gut–brain axis in a songbird

Recent research in mammals supports a link between cognitive ability and the gut microbiome, but little is known about this relationship in other taxa. In a captive population of 38 zebra finches (Taeniopygia guttata), we quantified performance on cognitive tasks measuring learning and memory. We sampled the gut microbiome via cloacal swab and quantified bacterial alpha and beta diversity. Performance on cognitive tasks related to beta diversity but not alpha diversity. We then identified differentially abundant genera influential in the beta diversity differences among cognitive performance categories. Though correlational, this study provides some of the first evidence of an avian microbiota–gut–brain axis, building foundations for future microbiome research in wild populations and during host development.     

果蝇长时程记忆缺陷型突变体的鉴定

长时程记忆作为依赖蛋白合成的记忆组分,对于了解高等认知活动的分子机制有着重要意义.与此同时,细胞粘连分子作为影响突触可塑性的重要因子在学习与记忆研究领域也日益得到重视.为探索作用于长时程记忆的细胞粘连分子,利用P因子在果蝇基因组随机插入制造突变体,并通过大规模行为筛选得到了一个可能的长时程记忆突变体RUO. 测序结果表明,突变体RUO的P因子位于果蝇中selectin超家族对应的furrowed同源基因功能片段和未知功能的CG1806基因编码片段之间,且更靠近furrowed片段.RT-PCR结果和互补遗传学实验均表明,突变体RUO主要影响furrowed基因的表达.为了进一步确认furrowed基因与长时程记忆的相关性,引入已知的furrowed基因突变体fw1.结果表明,fw1同样具有长时程记忆缺陷,同时具备正常的学习能力.荧光共聚焦扫描成像显示,该基因特异性的表达在果蝇大脑两个对称的未知神经元中.此项工作不仅证明了furrowed基因在果蝇长时程记忆中的重要作用,而且在解剖学上揭示了果蝇神经系统中可能参与长时程记忆形成的新的神经元.     

No evidence for an evolutionary trade-off between learning and immunity in a social insect

The immune response affects learning and memory in insects. Given this and the known fitness costs of both the immune system and learning, does an evolutionary trade-off exist between these two systems? We tested this by measuring the learning ability of 12 bumble-bee (Bombus terrestris) colonies in a free-flying paradigm. We then tested their immune response using the zone of inhibition assay. We found a positive relationship between colony learning performance and immune response, that is, fast-learning colonies also show high levels of antimicrobial activity. We conclude that there is no a priori reason to demand an evolutionary relationship between two traits that are linked physiologically.     

Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation

The incorporation of plant tolerance after damage as a new alternative to cope with herbivory, as opposed to resistance, opened new avenues for our understanding of coevolution between plants and herbivores. Although genetic variation on tolerance to defoliation has been detected in some species, few studies have been undertaken with nonagricultural species. In this study, we explore in the annual weed Datura stramonium the existence of genetic variation for tolerance and fitness costs of tolerance. To determine which fitness-related trait was responsible for possible differences in tolerance, growth rate, total flower and fruit production, and the number of seeds per fruit were recorded. Inbred line replicates of D. stramonium from a population of Mexico City were exposed to four defoliation levels (0%, 10%, 30%, and 70%). Our results from a greenhouse experiment using controlled genetic material (inbred lines) indicated that significant genetic variation for tolerance was detected across defoliation environments. Defoliation reduced plant fitness from 15% to 25% in the highest levels of defoliation. Differences on tolerance among inbred lines were accounted by a differential reduction in the proportion of matured fruits across defoliation levels (up to 20%). Within defoliation levels, significant genetic variation in plant fitness suggests that tolerance could be selected. The correlation between fitness values of inbred lines in two environments (with and without damage) was positive (rg = 0.77), but not significant, suggesting absence of fitness costs for tolerance. The finding of genetic variation on tolerance might be either due to differences among inbred lines in their capability to overcome foliar damage through compensation or due to costs incurred by inducing secondary metabolites. Our results indicate the potential for norms of reaction to be selected under a gradient of herbivory pressure and highlights the importance of dissecting induced from compensatory responses when searching for potential causes of genetic variation on tolerance.     

Individual variation in cognitive performance: developmental and evolutionary perspectives

Animal cognition experiments frequently reveal striking individual variation but rarely consider its causes and largely ignore its potential consequences. Studies often focus on a subset of high-performing subjects, sometimes viewing evidence from a single individual as sufficient to demonstrate the cognitive capacity of a species. We argue that the emphasis on demonstrating species-level cognitive capacities detracts from the value of individual variation in understanding cognitive development and evolution. We consider developmental and evolutionary interpretations of individual variation and use meta-analyses of data from published studies to examine predictors of individual performance. We show that reliance on small sample sizes precludes robust conclusions about individual abilities as well as inter- and intraspecific differences. We advocate standardization of experimental protocols and pooling of data between laboratories to improve statistical rigour. Our analyses show that cognitive performance is influenced by age, sex, rearing conditions and previous experience. These effects limit the validity of comparative analyses unless developmental histories are taken into account, and complicate attempts to understand how cognitive traits are expressed and selected under natural conditions. Further understanding of cognitive evolution requires efforts to elucidate the heritability of cognitive traits and establish whether elevated cognitive performance confers fitness advantages in nature.