Social environment mediates cancer progression in Drosophila

The influence of oncogenic phenomena on the ecology and evolution of animal species is becoming an important research topic. Similar to host–pathogen interactions, cancer negatively affects host fitness, which should lead to the selection of host control mechanisms, including behavioral traits that best minimize the proliferation of malignant cells. Social behavior is suggested to influence tumor progression. While the ecological benefits of sociality in gregarious species are widely acknowledged, only limited data are available on the role of the social environment on cancer progression. Here, we exposed adult Drosophila, with colorectal-like tumors, to different social environments. We show how subtle variations in social structure have dramatic effects on the progression of tumor growth. Finally, we reveal that flies can discriminate between individuals at different stages of tumor development and selectively choose their social environment accordingly. Our study demonstrates the reciprocal links between cancer and social interactions and how sociality may impact health and fitness in animals and its potential implications for disease ecology.This work was supported by the ANR (Blanc project EVOCAN to F.T. and project DROSONET to F.M. and C.S.), the CNRS (INEE and INSB), Fondation ARC (1555286 to J.M. and F.M.), The French league against Cancer (M27218 to J.M.), IDEEV program (to F.M.), by an International Associated Laboratory Project France/Australia, by the French-Australian Science Innovation Collaboration Program Early Career Fellowship (B.U.), by André Hoffmann (Fondation MAVA), Fyssen Foundation (to F.M. and E.H. D.) and the French Government (fellowship 2015–155 to M.D.)

Local Enhancement Promotes Cockroach Feeding Aggregations

Communication and learning from each other are part of the success of animal societies. Social insects invest considerable effort into signalling to their nestmates the locations of the most profitable resources in their environment. Growing evidence also indicates that insects glean such information through cues inadvertently provided by their conspecifics. Here, we investigate social information use in the foraging decisions by gregarious cockroaches (Blattella germanica L.). Individual cockroaches given a simultaneous choice in a Y-olfactometer between the odour of feeding conspecifics and the mixed odour of food plus non-feeding conspecifics showed a preference for the arm scented with the odour of feeding conspecifics. Social information (the presence of feeding conspecifics) was produced by cockroaches of all age classes and perceived at short distance in the olfactometer arms, suggesting the use of inadvertently provided cues rather than signals. We discuss the nature of these cues and the role of local enhancement (the selection of a location based on cues associated with the presence of conspecifics) in the formation of feeding aggregations in B. germanica. Similar cue-mediated recruitments could underpin a wide range of collective behaviours in group-living insects

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

Experimental Evolutionary Biology of Learning in “drosophila melanogaster”

La plupart des animaux, invertébrés inclus, ont la capacité de modifier leur comportement à la suite d'expériences, ils sont capables d'apprendre. Leur capacité d'apprentissage est elle-même un produit de l'évolution et le degré de modification d'un comportement par l'apprentissage varie selon les espèces et selon le comportement considéré. Pour un biologiste de l'évolution ceci soulève la question des conditions sous lesquelles les capacités d'apprentissage devraient évoluer. La façon selon laquelle la sélection naturelle favorise l'évolution des capacités d'apprentissage doit dépendre de la balance entre coûts et bénéfices liés à cette capacité. L'argument général est que l'apprentissage devrait être favorisé dans des environnements à fortes variations temporelles ou spatiales. En revanche, l'existence de coûts constitutifs ou induits pouvant contrecarrer cet avantage a été plusieurs fois postulé. Le thème général de cette thèse est l'étude des conditions environnementales sous lesquelles les capacités d'apprentissage devraient évoluer, des coûts et bénéfices associés à ces capacités et de l'impact de l'apprentissage dans l'évolution de la base innée du comportement. Afin de répondre à ces questions j'ai réalisé des expériences sur Drosophila melanogaster. Grâce à une approche d'évolution expérimentale j'ai sélectionné des drosophiles ayant une plus grande capacité d'apprentissage mettant ainsi en évidence la valeur adaptative de l'apprentissage en conditions environnementales variables. Cependant, ces drosophiles sélectionnées payent en retour un coût constitutif et un coût induit affectant leur fitness. Par un procédé similaire, je montre aussi que les capacités d'apprentissage peuvent évoluer dans un environnement constant et accélérer ou ralentir l'évolution des réponses innées. J'ai étudié cet effet en réalisant des simulations théoriques. En découplant le comportement en sa composante innée et sa composante acquise, ce travail met en évidence les conditions d'évolution de chaque composante ainsi que les interactions entre elles et la conséquence de ces interactions sur leur évolution respective.Many animals, including small invertebrates, have the capacity to modify their behaviour based on experience - they can learn. The ability to learn is itself a product of evolution, and the degree to which a given behaviour is modified by learning varies among species and among different types of behaviour. For an evolutionary biologist this raises the question of the conditions under which learning ability should evolve. The extent to which natural selection favours investment in developing learning ability will depend on the balance between costs and benefits of learning. On the one hand, it has been proposed that learning should be advantageous when the environment is temporally or spatially variable. On the other hand, constitutive or induced costs of learning have been repeatedly postulated and may counter select its evolution. The general aim of this PhD is to understand under which environmental conditions learning ability should evolve, what are the costs of learning ability and how an opportunity to learn influences the evolution of innate behaviour. To address these questions I carried out experimental work with Drosophila melanogaster. Under an experimental evolution set-up, I selected flies with higher learning ability and showed the adaptive value of learning under variable environment. However, lines selected for improved learning abilities pay constitutive and induced fitness costs associated with increased learning ability. I also present experimental evidence that learning ability can evolve under constant environment and accelerates or slows down the evolution of innate response. I investigated this effect with mathematical simulations. By decoupling the behaviour into its innate and learned component, this work provides evidence about the condition of evolution of each component and the evolutionary interaction between them

An operating cost of learning in Drosophila melanogaster

Although the fitness benefits of learning are well understood, we know little about its costs; yet both are essential to understand the evolution of animal learning. We tested the hypothesis that learning has an operating cost, such that an animal repeatedly forced to use its learning ability would show a reduction in some fitness component(s), relative to an animal of the same genotype that does not have to learn. Five ‘High-learning’ lines of Drosophila melanogaster, which had been selected for improved learning ability, were exposed to 12 consecutive 48-h cycles of alternating conditioning treatment under mild nutritional stress. Their learning score first increased, reaching a maximum around day 12 (i.e. the sixth conditioning cycle), and then progressively declined. These changes were not due to ageing, as they were not observed in flies from the same lines maintained under standard conditions. From around day 12, the productivity (egg-laying rate) of the flies in the conditioning treatment became progressively reduced, relative to flies from the same lines not exposed to conditioning, but otherwise kept under the same food-limited conditions. This reduction in productivity was not observed when these treatments were applied to five ‘Low-learning’ lines, which had not been exposed to selection, and which show no detectable response to conditioning under our experimental conditions. Furthermore, exposure to repeated cycles of conditioning revealed an apparent trade-off between the learning score and productivity among the ‘High-learning’ lines. These results indicate an operating cost of learning, paid only by genotypes that show learning, rather than general effects of stress caused by the conditioning regime. Potential proximate explanations include (1) the impairment of oviposition decisions caused by the accumulation of memory interference and (2) energy costs of collecting, processing and storing information

The effect of learning on experimental evolution of resource preference in Drosophila melanogaster

Learning is thought to be adaptive in variable environments, whereas constant, predictable environments are supposed to favor unconditional, genetically fixed responses. A dichotomous view of behavior as either learned or innate ignores a potential evolutionary interaction between the learned and innate components of a behavioral response. We addressed this interaction in the context of oviposition substrate choice in Drosophila melanogaster, asking two main questions. First, will learning also evolve in a constant environment in which it always pays to show the same choice? Second, how does an opportunity to learn affect the evolution of the innate (genetic) component of oviposition substrate choice? We exposed experimental populations to four selection regimes, involving selection on oviposition substrate preference (an orange versus a pineapple medium). In two selection regimes the flies were selected for preference either for the orange medium, or for the pineapple medium. In the remaining two selection regimes the flies were also selected for preference for either orange or pineapple, but additionally could use past experience (aversion learning) to decide which medium it paid to avoid. Lines exposed to the latter selection regimes evolved improved learning ability, indicating that learning may be advantageous even if the same behavioral response is favored every generation. Furthermore, of the two selection regimes that favored oviposition on the pineapple medium, the regime that allowed for learning led to the evolution of a stronger innate preference for pineapple, than the regime that did not allow for learning. In contrast, of the two regimes that selected for oviposition on the orange medium, the one that allowed for learning led to a smaller evolutionary change of the innate preference. Thus, an opportunity to learn facilitated the evolution of innate preference under selection for preference for pineapple, but hindered it under selection for preference for orange. We discuss possible mechanisms for this effect

A cost of long-term memory in Drosophila

Two distinct forms of consolidated associative memory are known in Drosophila: long- term memory and so-called anesthesia-resistant memory. Long-term memory is more stable, but unlike anesthesia-resistant memory, its formation requires protein synthesis. We show that flies induced to form long-term memory become more susceptible to extreme stress (such as desiccation). In contrast, induction of anesthesia-resistant memory had no detectable effect on desiccation resistance. This finding may help to explain why evolution has maintained anesthesia-resistant memory as another form of consolidated memory, distinct from long-term memory

Genetically idiosyncratic responses of Drosophila melanogaster populations to selection for improved learning ability

To what extent is adaptive evolution over short timescales repeatable? To address this question, we studied the performance of crosses between replicate Drosophila melanogaster lines previously subject to selection for improved learning response in the context of oviposition substrate choice. Of the 10 pairwise F1 crosses among the five selection lines, four performed in the original learning assay similarly to the parental lines, whereas the remaining six showed learning scores significantly below the average of the parental lines. In particular, four F1 crosses (three involving the same line) showed no detectable learning, on a par with unselected control lines. This indicates that the response to selection in some lines involved allelic substitutions at different loci. Additional assays of crosses between two selection lines indicated that the loss of performance in hybrids generalized to another type of learning assay, and held for both short- and long-term memory. Joint analysis of first- and second-generation crosses between these two lines supported the hypothesis that the response to selection in these different lines was based on the spread of recessive alleles at different loci. These results show that the evolutionary trajectories of populations of the same origin subject to uniform selection may sometimes diverge over very short evolutionary timescales

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