Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist

Food-caching corvids hide food, but such caches are susceptible to pilfering by other individuals. Consequently, the birds use several counter strategies to protect their caches from theft, e.g. hiding most of them out of sight. When observed by potential pilferers at the time of caching, experienced jays that have been thieves themselves, take further protective action. Once the potential pilferers have left, they move caches those birds have seen, re-hiding them in new places. Naive birds that had no thieving experience do not do so. By focusing on the counter strategies of the cacher when previously observed by a potential pilferer, these results raise the intriguing possibility that re-caching is based on a form of mental attribution, namely the simulation of another bird's viewpoint. Furthermore, the jays also keep track of the observer which was watching when they cached and take protective action accordingly, thus suggesting that they may also be aware of others' knowledge states.     

The genetic basis of spatial cognitive variation in a food-caching bird

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The evolution of animal 'cultures' and social intelligence

Decades-long field research has flowered into integrative studies that, together with experimental evidence for the requisite social learning capacities, have indicated a reliance on multiple traditions ('cultures') in a small number of species. It is increasingly evident that there is great variation in manifestations of social learning, tradition and culture among species, offering much scope for evolutionary analysis. Social learning has been identified in a range of vertebrate and invertebrate species, yet sustained traditions appear rarer, and the multiple traditions we call cultures are rarer still. Here, we examine relationships between this variation and both social intelligence--sophisticated information processing adapted to the social domain--and encephalization. First, we consider whether culture offers one particular confirmation of the social ('Machiavellian') intelligence hypothesis that certain kinds of social life (here, culture) select for intelligence: 'you need to be smart to sustain culture'. Phylogenetic comparisons, particularly focusing on our own study animals, the great apes, support this, but we also highlight some paradoxes in a broader taxonomic survey. Second, we use intraspecific variation to address the converse hypothesis that 'culture makes you smart', concluding that recent evidence for both chimpanzees and orangutans support this proposition.     

Social learning and evolution: the cultural intelligence hypothesis

If social learning is more efficient than independent individual exploration, animals should learn vital cultural skills exclusively, and routine skills faster, through social learning, provided they actually use social learning preferentially. Animals with opportunities for social learning indeed do so. Moreover, more frequent opportunities for social learning should boost an individual's repertoire of learned skills. This prediction is confirmed by comparisons among wild great ape populations and by social deprivation and enculturation experiments. These findings shaped the cultural intelligence hypothesis, which complements the traditional benefit hypotheses for the evolution of intelligence by specifying the conditions in which these benefits can be reaped. The evolutionary version of the hypothesis argues that species with frequent opportunities for social learning should more readily respond to selection for a greater number of learned skills. Because improved social learning also improves asocial learning, the hypothesis predicts a positive interspecific correlation between social-learning performance and individual learning ability. Variation among primates supports this prediction. The hypothesis also predicts that more heavily cultural species should be more intelligent. Preliminary tests involving birds and mammals support this prediction too. The cultural intelligence hypothesis can also account for the unusual cognitive abilities of humans, as well as our unique mechanisms of skill transfer.     

Game theory and the evolution of fearfulness in wild birds

When animals in a group live under predation threat, the fate of each individual depends on the way it reacts to danger, but also on the behaviour of its companions. Game theory should then help to understand the evolution of fearful behaviour in gregarious animals. To illustrate this approach, a model determines evolutionarily stable levels of fearfulness in bird flocks, assuming that flocks are the object of both predatory attacks and nonlethal disturbance. In the model, high levels of flightiness limit the risk of being killed by predators, but increase the amount of energy lost in flights during the season. The predicted levels of fearfulness are extremely variable. They depend on the respective frequencies of predatory attacks and simple disturbing events, and on the capacity of birds to detect and escape predators. These results may help to explain the variability of flightiness reported in birds.     

Cooperation and the evolution of intelligence

The high levels of intelligence seen in humans, other primates, certain cetaceans and birds remain a major puzzle for evolutionary biologists, anthropologists and psychologists. It has long been held that social interactions provide the selection pressures necessary for the evolution of advanced cognitive abilities (the 'social intelligence hypothesis'), and in recent years decision-making in the context of cooperative social interactions has been conjectured to be of particular importance. Here we use an artificial neural network model to show that selection for efficient decision-making in cooperative dilemmas can give rise to selection pressures for greater cognitive abilities, and that intelligent strategies can themselves select for greater intelligence, leading to a Machiavellian arms race. Our results provide mechanistic support for the social intelligence hypothesis, highlight the potential importance of cooperative behaviour in the evolution of intelligence and may help us to explain the distribution of cooperation with intelligence across taxa.     

Replay of Episodic Memories in the Rat

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Functional correlates of the lateral and medial entorhinal cortex: objects,path integration and local–global reference frames

The hippocampus receives its major cortical input from the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC). It is commonly believed that the MEC provides spatial input to the hippocampus, whereas the LEC provides non-spatial input. We review new data which suggest that this simple dichotomy between ‘where’ versus ‘what’ needs revision. We propose a refinement of this model, which is more complex than the simple spatial–non-spatial dichotomy. MEC is proposed to be involved in path integration computations based on a global frame of reference, primarily using internally generated, self-motion cues and external input about environmental boundaries and scenes; it provides the hippocampus with a coordinate system that underlies the spatial context of an experience. LEC is proposed to process information about individual items and locations based on a local frame of reference, primarily using external sensory input; it provides the hippocampus with information about the content of an experience.     

Investigating cognitive genetics and its implications for the treatment of cognitive deficit

Cognitive impairment in the elderly, caused by either normal ageing process or dementia, is an increasing problem in developed countries that has enormous social and economic considerations. Research investigating the genetic basis of cognition is a new and rapidly developing field that may aid in the development of new treatments for age-related cognitive deficit. Over the past 6 years, a number of quantitative trait loci (QTLs) have been associated with cognitive functioning in humans including loci within the genes catechol- o -methyltransferase, brain-derived neurotrophic factor, muscle segment homeobox 1, serotonin transporter 2A (HTR2A), cholinergic muscarinic receptor 2, cathepsin D, metabotrophic glutamate receptor and most recently the class II human leukocyte antigens. Unfortunately, inconsistency within the literature, which is a hallmark of almost all association studies investigating complex diseases and traits, is casting doubt as to which genes are truly associated with cognition and which are a result of Type 2 error. This review will highlight implicated intelligence QTLs, examine the probable reasons for the current discrepancies between reports and discuss the potential advantages that may be procured from the study of cognitive genetics.     

The role of wing length in the evolution of avian flightlessness

Flightlessness has evolved independently in at least 11 extant avian families. A number of hypotheses have been proposed to explain these transitions in individual families, including release from predation on oceanic islands, energetic costs of flight and use of forelimbs for activities other than flying. Few studies have sought to explore factors common to all families containing flightless species, which may explain the taxonomic distribution of flightlessness. In this study, we found that for all eight avian families which contain both flightless and flighted species, the flighted species have shorter wing lengths relative to body mass than their sister families. This result is not biased by taxon size. Models of avian aerodynamics predict that birds with relatively short wings pay a high energetic cost of flight. We suggest that these increased energetic costs of flying predispose these avian families to evolve flightless species. The various causes for the shortening of wings among flighted species of birds and the possibility of future transitions to flightlessness are discussed.     

The evolution of intelligence: adaptive specializations versus general process

Darwin argued that between-species differences in intelligence were differences of degree, not of kind. The contemporary ecological approach to animal cognition argues that animals have evolved species-specific and problem-specific processes to solve problems associated with their particular ecological niches: thus different species use different processes, and within a species, different processes are used to tackle problems involving different inputs. This approach contrasts both with Darwin's view and with the general process view, according to which the same central processes of learning and memory are used across an extensive range of problems involving very different inputs. We review evidence relevant to the claim that the learning and memory performance of non-human animals varies according to the nature of the stimuli involved. We first discuss the resource distribution hypothesis, olfactory learning-set formation, and the 'biological constraints' literature, but find no convincing support from these topics for the ecological account of cognition. We then discuss the claim that the performance of birds in spatial tasks of learning and memory is superior in species that depend heavily upon stored food compared to species that either show less dependence upon stored food or do not store food. If it could be shown that storing species enjoy a superiority specifically in spatial (and not non-spatial) tasks, this would argue that spatial tasks are indeed solved using different processes from those used in non-spatial tasks. Our review of this literature does not find a consistent superiority of storing over non-storing birds in spatial tasks, and, in particular, no evidence of enhanced superiority of storing species when the task demands are increased, by, for example, increasing the number of items to be recalled or the duration of the retention period. We discuss also the observation that the hippocampus of storing birds is larger than that of non-storing birds, and find evidence contrary to the view that hippocampal enlargement is associated with enhanced spatial memory; we are, however, unable to suggest a convincing alternative explanation for hippocampal enlargement. The failure to find solid support for the ecological view supports the view that there are no qualitative differences in cognition between animal species in the processes of learning and memory. We also argue that our review supports our contention that speculation about the phylogenetic development and function of behavioural processes does not provide a solid basis for gaining insight into the nature of those processes. We end by confessing to a belief in one major qualitative difference in cognition in animals: we believe that humans alone are capable of acquiring language, and that it is this capacity that divides our intelligence so sharply from non-human intelligence.     

Population genetic structure and its implications for adaptive variation in memory and the hippocampus on a continental scale in food-caching black-capped chickadees

Food-caching birds rely on stored food to survive the winter, and spatial memory has been shown to be critical in successful cache recovery. Both spatial memory and the hippocampus, an area of the brain involved in spatial memory, exhibit significant geographic variation linked to climate-based environmental harshness and the potential reliance on food caches for survival. Such geographic variation has been suggested to have a heritable basis associated with differential selection. Here, we ask whether population genetic differentiation and potential isolation among multiple populations of food-caching black-capped chickadees is associated with differences in memory and hippocampal morphology by exploring population genetic structure within and among groups of populations that are divergent to different degrees in hippocampal morphology. Using mitochondrial DNA and 583 AFLP loci, we found that population divergence in hippocampal morphology is not significantly associated with neutral genetic divergence or geographic distance, but instead is significantly associated with differences in winter climate. These results are consistent with variation in a history of natural selection on memory and hippocampal morphology that creates and maintains differences in these traits regardless of population genetic structure and likely associated gene flow.     

Dispersal capacity explains the evolution of lifespan variability

The evolutionary explanation for lifespan variation is still based on the antagonistic pleiotropy hypothesis, which has been challenged by several studies. Alternative models assume the existence of genes that favor aging and group benefits at the expense of reductions in individual lifespans. Here we propose a new model without making such assumptions. It considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species. We tested our model with individual‐based simulations and a comparative study using empirical data of maximum lifespan and natal dispersal distance in 26 species of birds, controlling for the effects of genetic variability, body size, and phylogeny. Simulations resulted in maximum lifespans arising from lowest dispersal probabilities, and comparative analyses resulted in a negative association between lifespan and natal dispersal distance, thus consistent with our model. Our findings therefore suggest that the evolution of lifespan variability is the result of the ecological process of dispersal.     

Inter‐specific brood parasitism and the evolution of avian reproductive strategies

Avian brood parasitism is a potent selective agent modulating host behaviors and morphology, although its role in determining diversification of avian breeding strategies remains elusive. Hitherto, the study of selection of brood parasites on host breeding strategies has been based on single reproductive trait approaches, which neglect that evolutionary responses to brood parasites may involve co‐ordinated changes in several aspects of reproduction. Here I consider covariation among reproductive traits to test whether parental breeding strategies of hosts of brown headed cowbird (BHC hereafter) in North America and the common cuckoo (CC hereafter) in Europe, two parasites with contrasting level of virulence, have evolved in response to brood parasitism. The effect of parasitism on avian breeding strategies differed between continents. Long term exposure to BHC parasitism selected for a lower breeding investment in North America, but not so CC parasitism in Europe. These results suggest a key role of parasite virulence on the evolution of avian breeding strategies and that brood parasitism has selected for a co‐ordinated breeding strategy of reducing parasitism costs by shortening and fractioning reproductive events within a single season in North America.     

Maternal immune factors and the evolution of secondary sexual characters

Secondary sexual characters have been hypothesized to revealthe ability of males to resist debilitating parasites. Althoughsuch reliable signaling of parasite resistance may be maintainedby parasite–host coevolution, maternal effects potentiallyprovide a previously neglected factor that could affect thelevel of genetic variation in resistance to parasites. Thatcould be the case because maternal effects have an entirelyenvironmental basis, or because they can maintain considerableamounts of genetic variation through epistatic effects, evenin the presence of strong directional selection. Maternal effectshave been shown to occur as maternal allocation of immune factorsto offspring, and such allocation may depend on the mating prospectsof sons, causing mothers to differentially allocate maternaleffects to eggs in species subject to intense sexual selection.Here we show that a maternal effect through innate antibacterialimmune defense, lysozyme, which is transferred from the motherto the egg in birds, is positively associated with the evolutionof secondary sexual characters. Previous studies have shownthat females differentially allocate lysozyme to their eggswhen mated to attractive males, and elevated levels of lysozymeare associated with reduced hatching failure and superior healthamong neonates and adults. In this study, comparative analysesof lysozyme from eggs of 85 species of birds showed a strongpositive relationship between brightness of male plumage andegg lysozyme, even when controlling for potentially confoundingvariables. These findings suggest that maternal immune factorsmay play a role in the evolution of secondary sexual characters.     

Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Insects harbour a wild diversity of symbionts that can spread and persist within populations by providing benefits to their host. The pea aphid Acyrthosiphon pisum maintains a facultative symbiosis with the bacterium Hamiltonella defensa, which provides enhanced resistance against the aphid parasitoid Aphidius ervi. Although the mechanisms associated with this symbiotic‐mediated protection have been investigated thoroughly, little is known about its evolutionary effects on parasitoid populations. We used an experimental evolution procedure in which parasitoids were exposed either to highly resistant aphids harbouring the symbiont or to low innate resistant hosts free of H. defensa. Parasitoids exposed to H. defensa gained virulence over time, reaching the same parasitism rate as those exposed to low aphid innate resistance only. A fitness reduction was associated with this adaptation as the size of parasitoids exposed to H. defensa decreased through generations. This study highlighted the considerable role of symbionts in host–parasite co‐evolutionary dynamics.