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The data and R scripts for our analyses are available at: https://github.com/olazl aure/PhosphorusPreference2022. They are archived on Figshare: https://doi.org/10.6084/m9.figshare.22032500; International audience; The broad variation in host use among polyphagous insects is well documented but still poorly understood. In numerous pest insects, the proximate mechanisms respon-sible for variation in oviposition preference among host plants remain to be eluci-dated. The invasive crop pest, Drosophila suzukii, attacks a wide range of host fruits. Females prefer ovipositing on particular fruit media (blackberry, cherry, blackcurrant) that are rich in phosphorus. As phosphorus is known to be involved in female repro-duction in insect species such as Drosophila, it could drive oviposition preference in D. suzukii. Phosphorus is either present as inorganic or organic phosphate in fruits. As the absolute content in macromolecules associated with phosphate in fruits (i.e. proteins and carbohydrates) do not affect oviposition in D. suzukii, we tested for the effect of inorganic phosphate on oviposition preference. We measured the egg- laying preferences of D. suzukii in a choice environment containing 12 artificial media with increasing content in inorganic phosphate (monopotassium dihydrogen phosphate). In our assay, D. suzukii females did not prefer ovipositing in media with high inorganic phosphate content compared to media with lower inorganic phosphate content. As a confirmation, we verified the previous result of a higher female preference for media made of phosphorus-rich fruits (blackberry, cherry, blackcurrant). The higher prefer-ence for phosphorus- rich fruits could be driven by macromolecules containing phos-phorus (e.g. phospholipids) or by the presence of one or more molecules that do not contain phosphorus, but that happen to be correlated to fruit phosphorus content. Studying the proximate mechanisms driving host use will ultimately help improve the management of D. suzukii and other crop pests

The broad variation in host use among polyphagous insects is well documented but still poorly understood. In numerous pest insects, the proximate mechanisms responsible for variation in oviposition preference among host plants remain to be elucidated. The invasive crop pest,Drosophila suzukii, attacks a wide range of host fruits. Females prefer ovipositing on particular fruit media (blackberry, cherry, blackcurrant) that are rich in phosphorus. As phosphorus is known to be involved in female reproduction in insect species such as Drosophila, it could drive oviposition preference inD. suzukii. Phosphorus is either present as inorganic or organic phosphate in fruits. As the absolute content in macromolecules associated with phosphate in fruits (i.e. proteins and carbohydrates) do not affect oviposition inD. suzukii, we tested for the effect of inorganic phosphate on oviposition preference. We measured the egg-laying preferences ofD. suzukiiin a choice environment containing 12 artificial media with increasing content in inorganic phosphate (monopotassium dihydrogen phosphate). In our assay,D. suzukiifemales did not prefer ovipositing in media with high inorganic phosphate content compared to media with lower inorganic phosphate content. As a confirmation, we verified the previous result of a higher female preference for media made of phosphorus-rich fruits (blackberry, cherry, blackcurrant). The higher preference for phosphorus-rich fruits could be driven by macromolecules containing phosphorus (e.g. phospholipids) or by the presence of one or more molecules that do not contain phosphorus, but that happen to be correlated to fruit phosphorus content. Studying the proximate mechanisms driving host use will ultimately help improve the management ofD. suzukiiand other crop pests.

bioRxiv 717702 ver. 3 Ce rapport est disponible dans : Peer Community in Evolutionary Biology; Environmentally acquired microbial symbionts could contribute to host adaptation to local conditions like vertically transmitted symbionts do. This scenario necessitates symbionts to have different effects in different environments. We investigated this idea in Drosophila melanogaster, a species which communities of bacterial symbionts vary greatly among environments.We isolatedfour bacterial strains isolated from the feces of a D. melanogasterlaboratory strain and tested their effects in two conditions:the ancestral environment (i.e. the laboratory medium) and a new environment (i.e. fresh fruit with live yeast). All bacterial effects on larval and adult traits differed among environments, ranging from very beneficial to marginally deleterious. The joint analysis of larval development speed and adult size further shows bacteria affected developmental plasticity more than resource acquisition. This effect was largely driven by the contrasted effects of the bacteria in each environment. Our study illustrates that understanding D. melanogastersymbiotic interactions in the wild will necessitate working in ecologically realistic conditions. Besides, context-dependent effects of symbionts, and their influence on host developmental plasticity, shed light on howenvironmentally acquired symbionts may contribute to host evolution.Keywords:symbiosis; extracellular bacteria; Drosophila melanogaster; life history traits; developmentalplasticity; resource acquisition

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, while 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.Impact SummaryNatural populations often exhibit good “fit” to the environment they are in. However, environments change over time and space, and following change, the fit between a population and its environment may be poor. A question of long-standing interest is how do populations track changing environments to maintain fitness? Two main mechanisms are known: (i) genetic shifts in the form of local adaptation, in which traits evolve over time through differences in fitness of individuals harboring different genetic variants, and (ii) plastic shifts, or adaptive phenotypic plasticity, in which traits immediately change in response to environmental change. Adaptation is common when environments change over multiple generations, while plasticity is common when environments change over an individual’s lifetime. However, it remains unclear whether plasticity or adaptation is more vital to maintaining fitness when environments change at an intermediate pace.Drosophila suzukii is well-suited to evaluating the relative importance of plasticity and adaptation in response to an intermediate pace of environmental change. This invasive pest species experiences an environment that shifts every 1-4 generations as host fruits change over time and space. Here, we studied natural populations of D. suzukii collected from different hosts. Using reciprocal common environment experiments, we evaluated their fitness on their source and alternative hosts.Drosophila suzukii populations were most fit on their source host, successfully tracking an intermediate pace of environmental change. We developed a statistical method to quantify the contributions of adaptive plasticity and local adaptation in determining fitness. We found that fitness was mainly maintained through local adaptation to each new host in succession. This study highlights that spatially and temporally variable selection does not prevent local adaptation and, on the contrary, illustrates how rapid the adaptive process can be. It also provides a novel statistical tool that can be applied to other systems

Little is known on the origin and maintenance of symbionts associated with Drosophila larvae in natura, which restricts the understanding of Drosophila-extracellular microorganism symbiosis in the light of evolution. Here, we studied the origin and maintenance of symbionts of Drosophila larvae under ecologically realistic conditions, to our knowledge for the first time, using yeast and bacterial isolates and two Drosophila species: the model organism D. melanogaster and the invasive pest D. suzukii. We discovered that Drosophila females and males both transmit yeast and bacteria symbionts to larvae. In addition, several symbiotic yeasts initially associated with larvae were conserved throughout host life cycle and transmitted to offspring. Our results suggest that stable associations of Drosophila flies with bacteria and yeasts may exist in natura and constitute a step forward in the understanding of wild Drosophila-microorganism symbioses.

Interactions between microbial symbionts of metazoan hosts are emerging as key features of symbiotic systems. Little is known about the role of such interactions on the maintenance of symbiosis through host’s life cycle. We studied the influence of symbiotic bacteria on the maintenance of symbiotic yeast through metamorphosis of the fly Drosophila melanogaster. To this end we mimicked the development of larvae in natural fruit. In absence of bacteria yeast was never found in young adults. However, yeast could maintain through metamorphosis when larvae were inoculated with symbiotic bacteria isolated from D. melanogaster faeces. Furthermore, an Enterobacteriaceae favoured yeast transstadial maintenance. Because yeast is a critical symbiont of D. melanogaster flies, bacterial influence on host-yeast association may have consequences for the evolution of insect-yeast-bacteria tripartite symbiosis and their cooperation.Summary statementBacterial symbionts of Drosophila influence yeast maintenance through fly metamorphosis, a novel observation that may have consequences for the evolution of insect-yeast-bacteria interactions.

Species that share resources often avoid competition with context-dependent behaviors. This is the case for the invasive insect pest Drosophila suzukii, whose larval ecological niche overlaps with that of Drosophila melanogaster in ripe, but not rotten, fruit. We discovered D. suzukii females prevent costly interspecific larval competition by avoiding oviposition on substrates previously visited by D. melanogaster. More precisely, D. melanogaster association with gut bacteria of the genus Lactobacillus triggers D. suzukii avoidance. However, D. suzukii avoidance behavior is condition-dependent, and D. suzukii females that themselves carry D. melanogaster bacteria stop avoiding sites visited by D. melanogaster. The adaptive significance of avoiding cues from the competitor’s microbiota was revealed by experimentally reproducing in-fruit larval competition: reduced survival of D. suzukii larvae was dependent on the presence of gut bacteria in the competitor. This study unveils a new role for the symbiotic microbiota and plastic behaviors in mediating interspecific competition.

Interactions between microbial symbionts influence their demography and that of their hosts. Taylor’s power law (TL)–a well-established relationship between population size mean and variance across space and time–may help to unveil the factors and processes that determine symbiont multiplications. Recent studies suggest pervasive interactions between symbionts inDrosophila melanogaster. We used this system to investigate theoretical predictions regarding the effects of interspecific interactions on TL parameters. We assayed twenty natural strains of bacteria in the presence and absence of a strain of yeast using an ecologically realistic set-up withD.melanogasterlarvae reared in natural fruit. Yeast presence led to a small increase in bacterial cell numbers; bacterial strain identity largely affected yeast multiplication. The spatial version of TL held among bacterial and yeast populations with slopes of 2. However, contrary to theoretical prediction, the facilitation of bacterial symbionts by yeast had no detectable effect on TL’s parameters. These results shed new light on the nature ofD.melanogaster’s symbiosis with yeast and bacteria. They further reveal the complexity of investigating TL with microorganisms.

Many symbionts provide nutrients to their host and/or affect its phenotypic plasticity. Such symbiont effects on host resource acquisition and allocation are often simultaneous and difficult to disentangle. Here we partitioned symbiont effects on host resource acquisition and allocation using a new framework based on the analysis of a well-established trade-off between host fitness components. This framework was used to analyze the effect of symbiotic yeast on the larval development of Drosophila larvae in field-realistic conditions. The screening of eighteen yeast fresh isolates showed they had similar effects on the resource acquisition in Drosophila melanogaster, D. simulans and D. suzukii but species-specific effects on resource allocation between either larval development speed or adult size. These differences shed light on the ecology of Drosophila flies and illustrate why distinguishing between these qualitatively different effects of microorganisms on hosts is essential to understand and predict symbiosis evolution.

1. Insect herbivores choose their food according to its protein to carbohydrate ratio, but the reasons why different species have contrasting intake targets remain unclear. According to the growth rate hypothesis, P-rich insects have higher growth rates. It is therefore expected that P-rich insects will prefer plants that are high in protein (hence in nitrogen, N) and phosphorus (P). 2. To test this hypothesis, the ecological stoichiometry and the interaction network frameworks were combined. The food preferences of 24 plant species by 23 grasshopper species were determined, and the N and P contents of both trophic levels were measured. The weighted mean P and N contents of the consumed plants, which represent the grasshoppers' feeding niche, were highly correlated, indicating that the grasshoppers' diets are spread along a single functional niche axis. The links between the stoichiometry of the plants and their consumers were then tested with the fourth corner analysis, a multivariate technique combining the plant traits, the insect traits and the interaction network. 3. In line with the earlier hypothesis, P-rich grasshoppers consumed plants high in N and P, probably because their growth rate is higher. These findings therefore introduce a mechanism that accounts for interspecific differences in diet preference. They also contribute to an understanding of how herbivore communities might respond to P and N limitation in ecosystems, and how complex interaction networks can influence biogeochemical cycles of N and P.

National audience

Environmentally acquired microbial symbionts could contribute to host adaptation to local adaptation like vertically transmitted symbionts do. This scenario necessitates symbionts to have different effects in different environments. In Drosophila melanogaster, communities of extracellular bacterial symbionts vary largely among environments, which could be due to variable effects on phenotype. We investigated this idea with four bacterial strains isolated from the feces of a D. melanogaster lab strain, and tested their effects in two environments: the environment of origin (i.e. the laboratory medium) and a new one (i.e. fresh fruit with live yeast). All bacterial effects on larval and adult traits differed among environments, ranging from very beneficial to marginally deleterious. The joint analysis of larval development speed and adult size further suggests bacteria would affect developmental plasticity more than resource acquisition in males. The context-dependent effects of bacteria we observed, and its underlying mechanisms, sheds light on how environmentally acquired symbionts may contribute to host evolution.

How do invasive pests affect interactions between members of pre-existing agrosystems? The invasive pest Drosophila suzukii is suspected to be involved in the aetiology of sour rot, a grapevine disease that otherwise develops following Drosophila melanogaster infestation of wounded berries. We combined field observations with laboratory assays to disentangle the relative roles of both Drosophila in disease development. We observed the emergence of numerous D. suzukii , but no D. melanogaster flies, from bunches that started showing mild sour rot symptoms days after field collection. However, bunches that already showed severe rot symptoms in the field mostly contained D. melanogaster . In the laboratory, oviposition by D. suzukii triggered sour rot development. An independent assay showed the disease increased grape attractiveness to ovipositing D. melanogaster females. Our results suggest that in invaded vineyards, D. suzukii facilitates D. melanogaster infestation and, consequently, favours sour rot outbreaks. Rather than competing with close species, the invader subsequently permits their reproduction in otherwise non-accessible resources and may cause more frequent, or more extensive, disease outbreaks.

Dataset for manuscript "Biological warfare between Drosophila species hints for sustainable crop protection" to be submitted.