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.

Cancer brings forward oviposition in the fly Drosophila melanogaster.

Hosts often accelerate their reproductive effort in response to a parasitic infection, especially when their chances of future reproduction decrease with time from the onset of the infection. Because malignancies usually reduce survival, and hence potentially the fitness, it is expected that hosts with early cancer could have evolved to adjust their life-history traits to maximize their immediate reproductive effort. Despite the potential importance of these plastic responses, little attention has been devoted to explore how cancers influence animal reproduction. Here, we use an experimental setup, a colony of genetically modified flies Drosophila melanogaster which develop colorectal cancer in the anterior gut, to show the role of cancer in altering life-history traits. Specifically, we tested whether females adapt their reproductive strategy in response to harboring cancer. We found that flies with cancer reached the peak period of oviposition significantly earlier (i.e., 2 days) than healthy ones, while no difference in the length and extent of the fecundity peak was observed between the two groups of flies. Such compensatory responses to overcome the fitness-limiting effect of cancer could explain the persistence of inherited cancer-causing mutant alleles in the wild.

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.

Sexual harassment induces a temporary fitness cost but does not constrain the acquisition of environmental information in fruit flies.

Across animals, sexual harassment induces fitness costs for females and males. However, little is known about the cognitive costs involved, i.e. whether it constrains learning processes, which could ultimately affect an individual's fitness. Here we evaluate the acquisition of environmental information in groups of fruit flies challenged with various levels of male sexual harassment. We show that, although high sexual harassment induces a temporary fitness cost for females, all fly groups of both sexes exhibit similar levels of learning. This suggests that, in fruit flies, the fitness benefits of acquiring environmental information are not affected by the fitness costs of sexual harassment, and that selection may favour cognition even in unfavourable social contexts. Our study provides novel insights into the relationship between sexual conflicts and cognition and the evolution of female counterstrategies against male sexual harassment.

Ecology of information: social transmission dynamics within groups of non-social insects.

While many studies focus on how animals use public information, the dynamics of information spread and maintenance within groups, i.e. the 'ecology of information', have received little attention. Here we use fruitflies trained to lay eggs on specific substrates to implement information into groups containing both trained and untrained individuals. We quantify inter-individual interactions and then measure the spread of oviposition preference with behavioural tests. Untrained individuals increase their interactive approaches in the presence of trained individuals, and the oviposition preference transmission is directly proportional to how much trained and untrained individuals interact. Unexpectedly, the preference of trained individuals to their trained oviposition substrate decreases after interactions with untrained individuals, leading to an overall informational loss. This shows that social learning alone is not enough to support informational stability.

Social environment influences performance in a cognitive task in natural variants of the foraging gene.

In Drosophila melanogaster, natural genetic variation in the foraging gene affects the foraging behaviour of larval and adult flies, larval reward learning, adult visual learning, and adult aversive training tasks. Sitters (for(s)) are more sedentary and aggregate within food patches whereas rovers (for(R)) have greater movement within and between food patches, suggesting that these natural variants are likely to experience different social environments. We hypothesized that social context would differentially influence rover and sitter behaviour in a cognitive task. We measured adult rover and sitter performance in a classical olfactory training test in groups and alone. All flies were reared in groups, but fly training and testing were done alone and in groups. Sitters trained and tested in a group had significantly higher learning performances compared to sitters trained and tested alone. Rovers performed similarly when trained and tested alone and in a group. In other words, rovers learning ability is independent of group training and testing. This suggests that sitters may be more sensitive to the social context than rovers. These differences in learning performance can be altered by pharmacological manipulations of PKG activity levels, the foraging (for) gene's gene product. Learning and memory is also affected by the type of social interaction (being in a group of the same strain or in a group of a different strain) in rovers, but not in sitters. These results suggest that for mediates social learning and memory in D. melanogaster.

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.

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.

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.