Frederic Mery

Natural polymorphism affecting learning and memory in Drosophila

Knowing which genes contribute to natural variation in learning and memory would help us understand how differences in these cognitive traits evolve among populations and species. We show that a natural polymorphism at the foraging (for) locus, which encodes a cGMP-dependent protein kinase (PKG), affects associative olfactory learning in Drosophila melanogaster. In an assay that tests the ability to associate an odor with mechanical shock, flies homozygous for one natural allelic variant of this gene (forR) showed better short-term but poorer long-term memory than flies homozygous for another natural allele (fors). The fors allele is characterized by reduced PKG activity. We showed that forR-like levels of both short-term learning and long-term memory can be induced in fors flies by selectively increasing the level of PKG in the mushroom bodies, which are centers of olfactory learning in the fly brain. Thus, the natural polymorphism at for may mediate an evolutionary tradeoff between short- and long-term memory. The respective strengths of learning performance of the two genotypes seem coadapted with their effects on foraging behavior: forR flies move more between food patches and so could particularly benefit from fast learning, whereas fors flies are more sedentary, which should favor good long-term memory.

Behavioural plasticity: an interaction between evolution and experience

Animals adjust their behaviour in response to complex environmental conditions. This form of plasticity requires the formation of association between information and an appropriate behavioural response. Such a connection is the result of a complex interaction between evolutionary pre-programmed cue-response behaviour (innate behavioural response) and cumulated lifetime experience (learning). The evolution of learning and innate behavioural responses is likely to depend on their respective fitness costs and benefits. However, as natural selection will indirectly affect each form through global behavioural plasticity, it is critical to understand how each form interacts with the other. The inclusion of innate behavioural plasticity and learning in behaviour is likely to result in more than the mere sum of each plastic form. In this review we investigate the costs and benefits of learning and innate behavioural responses and the effect of one on the other in their evolution. We highlight the need for more explicit study of the interaction between innate behavioural response and learning in natural systems for a better understanding of behavioural plasticity.

Spread of Social Information and Dynamics of Social Transmission within Drosophila Groups

Understanding how behavioral diversity arises and is maintained is central to evolutionary biology. Genetically based inheritance has been a predominant research focus of the last century; however, nongenetic inheritance, such as social transmission, has become a topic of increasing interest [1]. How social information impacts behavior depends on the balance between information gathered directly through personal experience versus that gleaned through social interactions and on the diffusion of this information within groups [2, 3]. We investigate how female Drosophila melanogaster use social information under seminatural conditions and whether this information can spread and be maintained within a group, a prerequisite for establishing behavioral transmission [4]. We show that oviposition site choice is heavily influenced by previous social interactions. Naive observer flies develop a preference for the same egg-laying medium as experienced demonstrator flies conditioned to avoid one of two equally rewarding media. Surprisingly, oviposition site preference was socially transmitted from demonstrators to observers even when they interacted in a cage with only unflavored, pure agar medium, and even when the observer flies had previous personal experience with both rewarding media. Our findings shed light on the diffusion process of social information within groups, on its maintenance, and ultimately, on the roots of behavioral local adaptation.

Costs of memory: lessons from ‘mini’ brains

Variation in learning and memory abilities among closely related species, or even among populations of the same species, has opened research into the relationship between cognition, ecological context and the fitness costs, and benefits of learning and memory. Such research programmes have long been dominated by vertebrate studies and by the assumption of a relationship between cognitive abilities, brain size and metabolic costs. Research on these ‘large brained’ organisms has provided important insights into the understanding of cognitive functions and their adaptive value. In the present review, we discuss some aspects of the fitness costs of learning and memory by focusing on ‘mini-brain’ studies. Research on learning and memory in insects has challenged some traditional positions and is pushing the boundaries of our understanding of the evolution of learning and memory.

Natural variation in learning and memory

Learning is widespread in the animal kingdom. From the small nematode worm Caenorhabditis elegans to humans, learning appears to play a central role in adaptation to local spatial and temporal environmental conditions. Though the neurobiological mechanisms of learning and memory have been intensively studied, the function and adaptive significance of learning has only recently received interest. Using learning, animals may progressively adjust their behavior in response to new environmental conditions, suggesting benefits of learning on animal performance, at least in the short term. How does learning affect the overall fitness of an animal? What are the fitness benefits and costs of learning? How can we explain the natural variation in learning ability observed between individuals, between populations of the same species or between closely related species? What are the ecological circumstances that favor the evolution of learning? There are all emerging questions that are central to a better understanding of the evolution of cognition and animal adaptation. Here I review the recent evidence showing that learning and memory are molded by an animals lifestyle within its ecological niche.

Gene–environment interplay in Drosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

Early life adversity has known impacts on adult health and behavior, yet little is known about the gene–environment interactions (GEIs) that underlie these consequences. We used the fruit fly Drosophila melanogaster to show that chronic early nutritional adversity interacts with rover and sitter allelic variants of foraging (for) to affect adult exploratory behavior, a phenotype that is critical for foraging, and reproductive fitness. Chronic nutritional adversity during adulthood did not affect rover or sitter adult exploratory behavior; however, early nutritional adversity in the larval period increased sitter but not rover adult exploratory behavior. Increasing for gene expression in the mushroom bodies, an important center of integration in the fly brain, changed the amount of exploratory behavior exhibited by sitter adults when they did not experience early nutritional adversity but had no effect in sitters that experienced early nutritional adversity. Manipulation of the larval nutritional environment also affected adult reproductive output of sitters but not rovers, indicating GEIs on fitness itself. The natural for variants are an excellent model to examine how GEIs underlie the biological embedding of early experience.

Use of Spatial Information and Search Strategies in a Water Maze Analog in Drosophila melanogaster

Learning the spatial organization of the environment is crucial to fitness in most animal species. Understanding proximate and ultimate factors underpinning spatial memory is thus a major goal in the study of animal behavior. Despite considerable interest in various aspects of its behavior and biology, the model species Drosophila melanogaster lacks a standardized apparatus to investigate spatial learning and memory. We propose here a novel apparatus, the heat maze, conceptually based on the Morris water maze used in rodents. Using the heat maze, we demonstrate that D. melanogaster flies are able to use either proximal or distal visual cues to increase their performance in navigating to a safe zone. We also show that flies are actively using the orientation of distal visual cues when relevant in targeting the safe zone, i.e., Drosophila display spatial learning. Parameter-based classification of search strategies demonstrated the progressive use of spatially precise search strategies during learning. We discuss the opportunity to unravel the mechanistic and evolutionary bases of spatial learning in Drosophila using the heat maze.

A natural genetic polymorphism affects retroactive interference in Drosophila melanogaster

As environments change, animals update their internal representations of the external world. New information about the environment is learned and retained whereas outdated information is disregarded or forgotten. Retroactive interference (RI) occurs when the retrieval of previously learned information is less available owing to the acquisition of recently acquired information. Even though RI is thought to be a major cause of forgetting, its functional significance is still under debate. We find that natural allelic variants of the Drosophila melanogaster foraging gene known to affect rover and sitter behaviour differ in RI. More specifically, rovers who were previously shown to experience greater environmental heterogeneity while foraging display RI whereas sitters do not. Rover responses are biased towards more recent learning events. These results provide an ecological context to investigate the function of forgetting via RI and a suitable genetic model organism to address the evolutionary relevance of cognitive tasks.

Experimental Evolution of Olfactory Memory in Drosophila melanogaster

In order to address the nature of genetic variation in learning performance, we investigated the response to classical olfactory conditioning in “high‐learning” Drosophila melanogaster lines previously subject to selection for the ability to learn an association between the flavor of an oviposition medium and bitter taste. In a T‐maze choice test, the seven high‐learning lines were better at avoiding an odor previously associated with aversive mechanical shock than were five unselected “low‐learning” lines originating from the same natural population. Thus, the evolved improvement in learning ability of high‐learning lines generalized to another aversion learning task involving a different aversive stimulus (shock instead of bitter taste) and a different behavioral context than that used to impose selection. In this olfactory shock task, the high‐learning lines showed improvements in the learning rate as well as in two forms of consolidated memory: anesthesia‐resistant memory and long‐term memory. Thus, genetic variation underlying the experimental evolution of learning performance in the high‐learning lines affected several phases of memory formation in the course of olfactory aversive learning. However, the two forms of consolidated memory were negatively correlated among replicate high‐learning lines, which is consistent with a recent hypothesis that these two forms of consolidated memory are antagonistic.

Aging and its differential effects on consolidated memory forms in Drosophila.

Aging is known to be associated with a decrease of learning and memory. Little is known on the specificity of this process. In Drosophila, two forms of consolidated memory have been observed. Anesthesia-resistant memory (ARM) is formed after one or several consecutive training sessions whereas long-term memory (LTM) is formed only after multiple training sessions separated in time. Both memory forms last more than 24 h. In the present experiment I, address the question of the effect of aging on the formation of each memory form. Twenty four hours after being conditioned, old flies show similar ARM as young flies but LTM was completely abolished. Age memory impairment seems therefore to be specific to one consolidated memory form.