Metabolic consequences of various fruit-based diets in a generalist insect species.

Most phytophagous insect species exhibit a limited diet breadth and specialize on a few or a single host plant. In contrast, some species display a remarkably large diet breadth, with host plants spanning several families and many species. It is unclear, however, whether this phylogenetic generalism is supported by a generic metabolic use of common host chemical compounds ('metabolic generalism') or alternatively by distinct uses of diet-specific compounds ('multi-host metabolic specialism')? Here, we simultaneously investigated the metabolomes of fruit diets and of individuals of a generalist phytophagous species, Drosophila suzukii, that developed on them. The direct comparison of metabolomes of diets and consumers enabled us to disentangle the metabolic fate of common and rarer dietary compounds. We showed that the consumption of biochemically dissimilar diets resulted in a canalized, generic response from generalist individuals, consistent with the metabolic generalism hypothesis. We also showed that many diet-specific metabolites, such as those related to the particular color, odor, or taste of diets, were not metabolized, and rather accumulated in consumer individuals, even when probably detrimental to fitness. As a result, while individuals were mostly similar across diets, the detection of their particular diet was straightforward. Our study thus supports the view that dietary generalism may emerge from a passive, opportunistic use of various resources, contrary to more widespread views of an active role of adaptation in this process. Such a passive stance towards dietary chemicals, probably costly in the short term, might favor the later evolution of new diet specializations.

Most insects that feed on green plants are specialists, meaning that they feed on just a narrow range of plant species. This reduces competition, especially if the host plant contains chemical deterrents that are toxic to other insects. But specialists cannot easily switch to feed on other plants, making them vulnerable to changes in the availability of the particular food type that they eat. Generalist insects, on the other hand, are able to consume a wide range of diets. This makes them more robust to changes in food availability, but it is unclear how these insects deal with the wider range of chemical compositions of their food. Do they convert food into energy using the same chemical process, or metabolism, for all the different things they eat? Or do generalists have a specific metabolic pathway for each food type? To answer this question, Olazcuaga, Baltenweck et al. studied the metabolism of a generalist fruit fly species. The team compared four types of fruit (blackcurrant, cherry, cranberry and strawberry) and isolated separate groups of flies so that they each ate only one type of fruit. By comparing the chemical composition of the flies with that of the fruit they ate, they were able to work out how each fruit type was metabolised. They found that the flies converted food into energy using the same process regardless of the type of fruit they ate. This lack of a specialist metabolic pathway for each fruit type meant that some chemicals were not metabolised and accumulated in the fly's body instead. This build-up of unprocessed chemicals is likely to be harmful to the fly. The results of Olazcuaga, Baltenweck et al. suggest that generalist insects do not actively adapt their metabolism to new food types. It's more likely that they try different types of food as the opportunity arises, regardless of the fact that some of the food will not be converted into energy and may harm them long term. These findings are important because they give us an insight into how the chemistry of a plant can shape the physiology of the organisms that consume it, and vice-versa. These insights are a crucial step in developing sustainable agriculture practices that must consider tackle how plants are pollinated, how plant seeds are dispersed and what type of pest control to use.

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly.

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry, and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants.

Faeces' odours attract gregarious locust hoppers.

Collective motion is one of the most impressive common features of gregarious locusts: once formed, bands and swarms get moving for long distances. It was shown that visual perception of neighbours plays a key role in maintaining marching behaviour at a local scale. But at a larger scale, mechanisms underlying band cohesion are less understood. It was shown in several field studies that individuals separated from the band were able to get back to the group, even after being separated since a night. In this context, faeces' odours could be a possible indicator of the recent passage of a group. In this study, we tested if nymphs are attracted by faeces' odours and if this effect is modulated by the age of the faeces. To this end, we conducted individual olfactometric behavioural assays of 3rd instar hoppers of desert locust, Schistocerca gregaria, exposed to odours of 1 h-old and 24 h-old faeces. We also used Gas Chromatography-Mass Spectrometry (GC-MS) to identify odours' volatile organic compounds from faeces. The results of behavioural assays indicated a strong attractive effect of faeces, with no preference for one of the two faecal age classes. Nymphs spent significantly more time in the side of the olfactometer where the faeces' odours came from, and 72.7% of tested individuals chose this side first. We filtered and annotated 11 volatile organic compounds present in both fresh and old faeces in GC-MS analyses, including guaiacol and phenol, which are known to cause an aggregative effect on desert locusts. As the attractive effect lasted over 24 h, band's faeces could still have an attractive effect when individuals are separated from the band since one day. In this situation, latecomers individuals would be able to get back to the group by following the traces of their predecessors.

Adaptation and correlated fitness responses over two time scales in Drosophila suzukii populations evolving in different environments.

The process of local adaptation involves differential changes in fitness over time across different environments. Although experimental evolution studies have extensively tested for patterns of local adaptation at a single time point, there is relatively little research that examines fitness more than once during the time course of adaptation. We allowed replicate populations of the fruit pest Drosophila suzukii to evolve in one of eight different fruit media. After five generations, populations with the highest initial levels of maladaptation had mostly gone extinct, whereas experimental populations evolving on cherry, strawberry and cranberry media had survived. We measured the fitness of each surviving population in each of the three fruit media after five and after 26 generations of evolution. After five generations, adaptation to each medium was associated with increased fitness in the two other media. This was also true after 26 generations, except when populations that evolved on cranberry medium developed on cherry medium. These results suggest that, in the theoretical framework of a fitness landscape, the fitness optima of cherry and cranberry media are the furthest apart. Our results show that studying how fitness changes across several environments and across multiple generations provides insights into the dynamics of local adaptation that would not be evident if fitness were analysed at a single point in time. By allowing a qualitative mapping of an experimental fitness landscape, our approach will improve our understanding of the ecological factors that drive the evolution of local adaptation in D. suzukii.

Oviposition Preference and Larval Performance of Drosophila suzukii (Diptera: Drosophilidae), Spotted-Wing Drosophila: Effects of Fruit Identity and Composition.

A better understanding of the factors affecting host plant use by spotted-wing drosophila (Drosophila suzukii) could aid in the development of efficient management tools and practices to control this pest. Here, proxies of both preference (maternal oviposition behavior) and performance (adult emergence) were evaluated for 12 different fruits in the form of purees. The effect of the chemical composition of the fruits on preference and performance traits was then estimated. We synthesized the literature to interpret our findings in the light of previous studies that measured oviposition preference and larval performance of D. suzukii. We show that fruit identity influences different parts of the life cycle, including oviposition preference under both choice and no-choice conditions, emergence rate, development time, and number of emerging adults. Blackcurrant was always among the most preferred fruit we used, while grape and tomato were the least preferred fruits. Larvae performed better in cranberry, raspberry, strawberry, and cherry than in the other fruits tested. We found that fruit chemical compounds can explain part of the effect of fruit on D. suzukii traits. In particular, oviposition preference under choice conditions was strongly influenced by fruit phosphorus content. In general, the consensus across studies is that raspberry, blackberry, and strawberry are among the best hosts while blackcurrant, grape and rose hips are poor hosts. Our results generally confirm this view but also suggest that oviposition preferences do not necessarily match larval performances. We discuss opportunities to use our results to develop new approaches for pest management.

The Genomic Basis of Color Pattern Polymorphism in the Harlequin Ladybird.

Many animal species comprise discrete phenotypic forms. A common example in natural populations of insects is the occurrence of different color patterns, which has motivated a rich body of ecological and genetic research [1-6]. The occurrence of dark, i.e., melanic, forms displaying discrete color patterns is found across multiple taxa, but the underlying genomic basis remains poorly characterized. In numerous ladybird species (Coccinellidae), the spatial arrangement of black and red patches on adult elytra varies wildly within species, forming strikingly different complex color patterns [7, 8]. In the harlequin ladybird, Harmonia axyridis, more than 200 distinct color forms have been described, which classic genetic studies suggest result from allelic variation at a single, unknown, locus [9, 10]. Here, we combined whole-genome sequencing, population-based genome-wide association studies, gene expression, and functional analyses to establish that the transcription factor Pannier controls melanic pattern polymorphism in H. axyridis. We show that pannier is necessary for the formation of melanic elements on the elytra. Allelic variation in pannier leads to protein expression in distinct domains on the elytra and thus determines the distinct color patterns in H. axyridis. Recombination between pannier alleles may be reduced by a highly divergent sequence of ∼170 kb in the cis-regulatory regions of pannier, with a 50 kb inversion between color forms. This most likely helps maintain the distinct alleles found in natural populations. Thus, we propose that highly variable discrete color forms can arise in natural populations through cis-regulatory allelic variation of a single gene.

Deciphering the Routes of invasion of Drosophila suzukii by Means of ABC Random Forest.

Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.

Introduced Drosophila subobscura populations perform better than native populations during an oviposition choice task due to increased fecundity but similar learning ability.

The success of invasive species is tightly linked to their fitness in a putatively novel environment. While quantitative components of fitness have been studied extensively in the context of invasive species, fewer studies have looked at qualitative components of fitness, such as behavioral plasticity, and their interaction with quantitative components, despite intuitive benefits over the course of an invasion. In particular, learning is a form of behavioral plasticity that makes it possible to finely tune behavior according to environmental conditions. Learning can be crucial for survival and reproduction of introduced organisms in novel areas, for example, for detecting new predators, or finding mates or oviposition sites. Here we explored how oviposition performance evolved in relation to both fecundity and learning during an invasion, using native and introduced Drosophila subobscura populations performing an ecologically relevant task. Our results indicated that, under comparable conditions, invasive populations performed better during our oviposition task than did native populations. This was because invasive populations had higher fecundity, together with similar cognitive performance when compared to native populations, and that there was no interaction between learning and fecundity. Unexpectedly, our study did not reveal an allocation trade-off (i.e., a negative relationship) between learning and fecundity. On the contrary, the pattern we observed was more consistent with an acquisition trade-off, meaning that fecundity could be limited by availability of resources, unlike cognitive ability. This pattern might be the consequence of escaping natural enemies and/or competitors during the introduction. The apparent lack of evolution of learning may indicate that the introduced population did not face novel cognitive challenges in the new environment (i.e., cognitive "pre-adaptation"). Alternatively, the evolution of learning may have been transient and therefore not detected.

Empirical assessment of RAD sequencing for interspecific phylogeny.

Next-generation sequencing opened up new possibilities in phylogenetics; however, choosing an appropriate method of sample preparation remains challenging. Here, we demonstrate that restriction-site-associated DNA sequencing (RAD-seq) generates useful data for phylogenomics. Analysis of our RAD library using current bioinformatic and phylogenetic tools produced 400× more sites than our Sanger approach (2,262,825 nt/species), fully resolving relationships between 18 species of ground beetles (divergences up to 17 My). This suggests that RAD-seq is promising to infer phylogeny of eukaryotic species, though potential biases need to be evaluated and new methodologies developed to take full advantage of such data.

Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata.

Androgenesis is the production of an offspring containing exclusively the nuclear genome of the fathering male via the maternal eggs. This unusual mating system is generally considered a male trait, giving to androgenetic males a substantial fitness advantage over their sexually reproducing relatives. We here provide the first empirical study of the evolutionary outcomes of androgenesis in a haplo-diploid organism: the invasive ant Wasmannia auropunctata. Some of the populations of this species have a classical haplo-diploid sexual mating system. In other populations, females and males are produced through parthenogenesis and androgenesis, respectively, whereas workers are produced sexually. We conducted laboratory reciprocal-cross experiments with reproductive individuals from both types of populations and analysed their progenies with genetic markers, to determine the respective contribution of males and females to the production of androgenetic males. We found that androgenesis was a parthenogenetic female trait. A population genetic study conducted in natura confirmed the parthenogenetic female origin of androgenesis, with the identification of introgression events of sexual male genotypes into androgenetic/parthenogenetic lineages. We argue that by producing males via androgenesis, parthenogenetic queen lineages may increase and/or maintain their adaptive potential, while maintaining the integrity of their own genome, by occasionally acquiring new male genetic material and avoiding inbreeding depression within the sexually produced worker cast.

Estimation of population allele frequencies from next-generation sequencing data: pool-versus individual-based genotyping.

Molecular markers produced by next-generation sequencing (NGS) technologies are revolutionizing genetic research. However, the costs of analysing large numbers of individual genomes remain prohibitive for most population genetics studies. Here, we present results based on mathematical derivations showing that, under many realistic experimental designs, NGS of DNA pools from diploid individuals allows to estimate the allele frequencies at single nucleotide polymorphisms (SNPs) with at least the same accuracy as individual-based analyses, for considerably lower library construction and sequencing efforts. These findings remain true when taking into account the possibility of substantially unequal contributions of each individual to the final pool of sequence reads. We propose the intuitive notion of effective pool size to account for unequal pooling and derive a Bayesian hierarchical model to estimate this parameter directly from the data. We provide a user-friendly application assessing the accuracy of allele frequency estimation from both pool- and individual-based NGS population data under various sampling, sequencing depth and experimental error designs. We illustrate our findings with theoretical examples and real data sets corresponding to SNP loci obtained using restriction site-associated DNA (RAD) sequencing in pool- and individual-based experiments carried out on the same population of the pine processionary moth (Thaumetopoea pityocampa). NGS of DNA pools might not be optimal for all types of studies but provides a cost-effective approach for estimating allele frequencies for very large numbers of SNPs. It thus allows comparison of genome-wide patterns of genetic variation for large numbers of individuals in multiple populations.

Thermotolerance adaptation to human-modified habitats occurs in the native range of the invasive ant Wasmannia auropunctata before long-distance dispersal.

Key evolutionary events associated with invasion success are traditionally thought to occur in the introduced, rather than the native range of species. In the invasive ant Wasmannia auropunctata, however, a shift in reproductive system has been demonstrated within the native range, from the sexual non-dominant populations of natural habitats to the clonal dominant populations of human-modified habitats. Because abiotic conditions of human- modified habitats are hotter and dryer, we performed lab experiments on workers from a set of native and introduced populations, to investigate whether these ecological and genetic transitions were accompanied by a change in thermotolerance and whether such changes occurred before establishment in the introduced range. Thermotolerance levels were higher in native populations from human-modified habitats than in native populations from natural habitats, but were similar in native and introduced populations from human-modified habitats. Differences in thermotolerance could not be accounted for by differences in body size. A scenario based on local adaptation in the native range before introduction in remote areas represents the most parsimonious hypothesis to account for the observed phenotypic pattern. These findings highlight the importance of human land use in explaining major contemporary evolutionary changes.

A genetic polymorphism affecting reliance on personal versus public information in a spatial learning task in Drosophila melanogaster.

Organisms that face behavioural challenges can use different types of information to guide their decisions. First, they can use the personal information they sample in their environment. Second, they can use the inadvertent social information provided by the behaviour of conspecifics or heterospecifics (i.e. public information). Currently, little is known about the interaction between genetic variation and the use of personal versus public information in natural populations. Here, we investigated whether a natural genetic polymorphism affects the use of personal versus public information in a spatial learning task in Drosophila melanogaster. We found that genetic variation at the foraging locus interacts with social context during spatial learning. While both allelic variants are able to use personal and public information to improve their navigation during 10 training trials, a probe trial revealed that individuals carrying the for(R) (rover) allele rely mainly on personal information, whereas individuals carrying the for(s) (sitter) allele either use or display more public information than rovers. Accordingly, transfer of social information is more important in groups of sitters than in groups of rovers. These results suggest that a positive feedback loop can occur between alleles promoting group living, such as for(s), and the use and/or display of public information, ultimately providing the opportunity for the joint evolution of sociality and cultural traits.

Distribution of endosymbiotic reproductive manipulators reflects invasion process and not reproductive system polymorphism in the little fire ant Wasmannia auropunctata.

Endosymbiotic reproductive manipulators may have drastic effects on the ecological and evolutionary dynamics of their hosts. The prevalence of these endosymbionts reflects both their ability to manipulate their hosts and the history of the host populations. The little fire ant Wasmannia auropunctata displays a polymorphism in both its reproductive system (sexual versus clonal populations) and the invasive status of its populations (associated to a habitat shift). We first screened for the presence of a diverse array of reproductive parasites in sexual and clonal populations of W. auropunctata, as a means to investigate the role of endosymbionts in reproductive phenotypes. Wolbachia was the only symbiont found and we then focused on its worldwide distribution and diversity in natural populations of W. auropunctata. Using a multilocus scheme, we further characterized the Wolbachia strains present in these populations. We found that almost all the native sexual populations and only a few clonal populations are infected by Wolbachia. The presence of similar Wolbachia strains in both sexual and clonal populations indicates that they are probably not the cause of the reproductive system polymorphism. The observed pattern seems rather associated to the invasion process of W. auropunctata. In particular, the observed loss of Wolbachia in clonal populations, that recurrently emerged from sexual populations, likely resulted from natural heat treatment and/or relaxed selection during the shift in habitat associated to the invasion process.

The effect of RAD allele dropout on the estimation of genetic variation within and between populations.

Inexpensive short-read sequencing technologies applied to reduced representation genomes is revolutionizing genetic research, especially population genetics analysis, by allowing the genotyping of massive numbers of single-nucleotide polymorphisms (SNP) for large numbers of individuals and populations. Restriction site-associated DNA (RAD) sequencing is a recent technique based on the characterization of genomic regions flanking restriction sites. One of its potential drawbacks is the presence of polymorphism within the restriction site, which makes it impossible to observe the associated SNP allele (i.e. allele dropout, ADO). To investigate the effect of ADO on genetic variation estimated from RAD markers, we first mathematically derived measures of the effect of ADO on allele frequencies as a function of different parameters within a single population. We then used RAD data sets simulated using a coalescence model to investigate the magnitude of biases induced by ADO on the estimation of expected heterozygosity and F(ST) under a simple demographic model of divergence between two populations. We found that ADO tends to overestimate genetic variation both within and between populations. Assuming a mutation rate per nucleotide between 10(-9) and 10(-8), this bias remained low for most studied combinations of divergence time and effective population size, except for large effective population sizes. Averaging F(ST) values over multiple SNPs, for example, by sliding window analysis, did not correct ADO biases. We briefly discuss possible solutions to filter the most problematic cases of ADO using read coverage to detect markers with a large excess of null alleles.

Where do adaptive shifts occur during invasion? A multidisciplinary approach to unravelling cold adaptation in a tropical ant species invading the Mediterranean area.

Evolution may improve the invasiveness of populations, but it often remains unclear whether key adaptation events occur after introduction into the recipient habitat (i.e. post-introduction adaptation scenario), or before introduction within the native range (i.e. prior-adaptation scenario) or at a primary site of invasion (i.e. bridgehead scenario). We used a multidisciplinary approach to determine which of these three scenarios underlies the invasion of the tropical ant Wasmannia auropunctata in a Mediterranean region (i.e. Israel). Species distribution models (SDM), phylogeographical analyses at a broad geographical scale and laboratory experiments on appropriate native and invasive populations indicated that Israeli populations followed an invasion scenario in which adaptation to cold occurred at the southern limit of the native range before dispersal to Israel. We discuss the usefulness of combining SDM, genetic and experimental approaches for unambiguous determination of eco-evolutionary invasion scenarios.

Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions.

Adaptive evolution is currently accepted as playing a significant role in biological invasions. Adaptations relevant to invasions are typically thought to occur either recently within the introduced range, as an evolutionary response to novel selection regimes, or within the native range, because of long-term adaptation to the local environment. We propose that recent adaptation within the native range, in particular adaptations to human-altered habitat, could also contribute to the evolution of invasive populations. Populations adapted to human-altered habitats in the native range are likely to increase in abundance within areas frequented by humans and associated with human transport mechanisms, thus enhancing the likelihood of transport to a novel range. Given that habitats are altered by humans in similar ways worldwide, as evidenced by global environmental homogenization, propagules from populations adapted to human-altered habitats in the native range should perform well within similarly human-altered habitats in the novel range. We label this scenario 'Anthropogenically Induced Adaptation to Invade'. We illustrate how it differs from other evolutionary processes that may occur during invasions, and how it can help explain accelerating rates of invasions.

Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers.

The little fire ant, Wasmannia auropunctata, displays a peculiar breeding system polymorphism. Classical haplo-diploid sexual reproduction between reproductive individuals occurs in some populations, whereas, in others, queens and males reproduce clonally. Workers are produced sexually and are sterile in both clonal and sexual populations. The evolutionary fate of the clonal lineages depends strongly on the underlying mechanisms allowing reproductive individuals to transmit their genomes to subsequent generations. We used several queen-offspring data sets to estimate the rate of transition from heterozygosity to homozygosity associated with recombination events at 33 microsatellite loci in thelytokous parthenogenetic queen lineages and compared these rates with theoretical expectations under various parthenogenesis mechanisms. We then used sexually produced worker families to define linkage groups for these 33 loci and to compare meiotic recombination rates in sexual and parthenogenetic queens. Our results demonstrate that queens from clonal populations reproduce by automictic parthenogenesis with central fusion. These same parthenogenetic queens produce normally segregating meiotic oocytes for workers, which display much lower rates of recombination (by a factor of 45) than workers produced by sexual queens. These low recombination rates also concern the parthenogenetic production of queen offspring, as indicated by the very low rates of transition from heterozygosity to homozygosity observed (from 0% to 2.8%). We suggest that the combination of automixis with central fusion and a major decrease in recombination rates allows clonal queens to benefit from thelytoky while avoiding the potential inbreeding depression resulting from the loss of heterozygosity during automixis. In sterile workers, the strong decrease of recombination rates may also facilitate the conservation over time of some coadapted allelic interactions within chromosomes that might confer an adaptive advantage in habitats disturbed by human activity, where clonal populations of W. auropunctata are mostly found.

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.

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.