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In an era marked by rapid global changes, the reinforcement and modernization of plant health surveillance systems have become imperative. Sixty-five scientists present here a research agenda for an enhanced and modernized plant health surveillance to anticipate and mitigate disease and pest emergence. Our approach integrates a wide range of scientific fields (from life, social, physical and engineering sciences) and identifies the key knowledge gaps, focusing on anticipation, risk assessment, early detection, and multi-actor collaboration. The research directions we propose are organized around four complementary thematic axes. The first axis is the anticipation of pest emergence, encompassing innovative forecasting, adaptive potential, and the effects of climatic and cropping system changes. The second axis addresses the use of versatile broad-spectrum surveillance tools, including molecular or imaging diagnostics supported by artificial intelligence, and monitoring generic matrices such as air and water. The third axis focuses on surveillance of known pests from new perspectives, i.e., using novel approaches to detect known species but also anticipating and detecting, within a species, the populations or genotypes that pose a higher risk. The fourth axis advocates the management of plant health as a commons through the establishment of multi-actor and cooperative surveillance systems for long-term data-driven alert systems and information dissemination. We stress the importance of integrating data and information from multiple sources through open science databases and metadata, alongside developing methods for interpolating and extrapolating incomplete data. Finally, we advocate an Integrated Health Surveillance approach in the One Health context, favoring tailored and versatile solutions to plant health problems and recognizing the interconnected risks to the health of plants, humans, animals and the environment, including food insecurity, pesticide residues, e

One promising avenue for reconciling the goals of crop production and ecosystem preservation consists in the manipulation of beneficial biotic interactions, such as between insects and microbes. Insect gut microbiota can affect host fitness by contributing to development, host immunity, nutrition, or behavior. However, the determinants of gut microbiota composition and structure, including host phylogeny and host ecology, remain poorly known. Here, we used a well-studied community of eight sympatric fruit fly species to test the contributions of fly phylogeny, fly specialization, and fly sampling environment on the composition and structure of bacterial gut microbiota. Comprising both specialists and generalists, these species belong to five genera from to two tribes of the Tephritidae family. For each fly species, one field and one laboratory samples were studied. Bacterial inventories to the genus level were produced using 16S metabarcoding with the Oxford Nanopore Technology. Sample bacterial compositions were analyzed with recent network-based clustering techniques. Whereas gut microbiota were dominated by the Enterobacteriaceae family in all samples, microbial profiles varied across samples, mainly in relation to fly identity and sampling environment. Alpha diversity varied across samples and was higher in the Dacinae tribe than in the Ceratitinae tribe. Network analyses allowed grouping samples according to their microbial profiles. The resulting groups were very congruent with fly phylogeny, with a significant modulation of sampling environment, and with a very low impact of fly specialization. Such a strong imprint of host phylogeny in sympatric fly species, some of which share much of their host plants, suggests important control of fruit flies on their gut microbiota through vertical transmission and/or intense filtering of environmental bacteria.

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.

Theory predicts that adaptive trade-offs across environments promote the evolution of specialized genotypes. However, generalist genotypes that are not better adapted to a specific environment are often observed in nature. Generalists can be maintained despite trade-offs between environments under two circumstances: when environmental conditions are variable spatially or temporally or when there is no genetic variability to evolve toward specialized genotypes. Drosophila suzukii is an insect pest that attacks the fruits of a wide range of host plants. The availability of each type of hast is restricted to a certain time of the year, which might prevent the evolution of specialist genotypes. We can hypothesize that if flies were able to develop on the same hast for multiple generations, increased specialization should arise. We tested this hypothesis using an experimental evolution approach. We maintained replicate populations of flies in three different fruit environments. After five generations of experimental selection, each population evolved increased fitness on the fruit it was maintained on as well as on the two other fruits. In addition, preference tests showed that lines did not prefer their own fruit environment. These results indicate that the populations adapted to laboratory conditions, and that there was no response to potential trade-offs across environments. This suggests, that such trade-offs are weak or that there is no genetic variation for specialization to evolve. To confirm this finding, we are maintaining the experimental lines for another five additional generations. Our preliminary results highlight the difficulty of studying the evolution of specialization.

The life-history traits of organisms can be driven by the environment. Specifically, the nutritional composition of resources can influence life-history traits in insects. In Drosophila, the ratio of protein to carbohydrate (the P:C ratio) strongly influences life history traits. However, natural resources used by Drosophila species vary in many other factors. We compare how well P:C ratios of fruit resources predict life history traits in , relative to other measures of fruit composition and fruit identity, which integrates all aspects of the resource. We evaluate how 12 different fruit purees influenced life-history traits in . Fecundity (eggs laid in 24 hours) on each fruit medium was measured in a choice and a nochoice environment. We also evaluated development time, the rate of survival from egg to adult, and the total number of adults as an estimate of total fitness. We then test whether fruit identity, composition or P:C ratio best predict life history. Fruit influenced the entire life cycle, including oviposition and larval performance as well as the number of adults produced in the next generation. Variation in these traits is best explained by fruit identity, then composition, and lastly by the P:C ratio. These results highlight the importance of considering a resource as a whole. Considering only the ratio of protein to carbohydrates is not sufficient for understanding variation in key life-history traits.

In simultaneous hermaphrodites, gender conflicts that arise from two potential mates sharing the same gender preference may be solved through conditional reciprocity (or gamete trading). Conditional reciprocity had initially been considered widespread, but recent studies suggest that its real occurrence may have been overestimated, possibly because most mating observations have been performed on isolated pairs of individuals. Some resulting patterns (e.g., non-random alternation of sexual roles) were indeed compatible with conditional reciprocity but could also have stemmed from the two partners independently executing their own mating strategy and being experimentally enforced to do so with the same partner. Non-random alternation of gender roles was recently documented in the simultaneously hermaphroditic freshwater snail Physa acuta. To distinguish between conditional and unconditional gender alternations, we observed copulations of individually marked snails reared at three contrasted densities. We showed that density affected the overall frequency of copulations during the first 2days of the experiment with high-density boxes showing more copulations than low density boxes, but it did not affect gender alternation patterns. A change in gender role was observed more often than expected by chance over two successive copulations by the same individual, confirming previous studies. However, gender switches did not preferentially occur with the same partner. We conclude that gender alternation is not due to conditional reciprocity in P. acuta. It may rather stem from each individual having a preference for gender alternation. We finally discuss the mechanisms and the potential extent of this unconditional reciprocity

Inbreeding depression should select for inbreeding avoidance behaviours. Here we test this hypothesis in two populations of the simultaneous hermaphroditic freshwater snail Physa acuta. We recorded the copulatory behaviour of 288 pairs of sib-mates, non-kin mates from the same population, or non-kin mates from two different populations. We find that kin discriminatory behaviours exist in this species, exclusively expressed by individuals playing the female role. We discuss the relevance of our finding in the context of the evolution of recognition systems and the consequences of such a behaviour in natural populations

Copper-based antimicrobial compounds are widely used to control plant bacterial pathogens. Pathogens have adapted in response to this selective pressure. Xanthomonas citri pv. citri, a major citrus pathogen causing Asiatic citrus canker, was first reported to carry plasmid-encoded copper resistance in Argentina. This phenotype was conferred by the copLAB gene system. The emergence of resistant strains has since been reported in Réunion and Martinique. Using microsatellite-based genotyping and copLAB PCR, we demonstrated that the genetic structure of the copper-resistant strains from these three regions was made up of two distant clusters and varied for the detection of copLAB amplicons. In order to investigate this pattern more closely, we sequenced six copper-resistant X. citri pv. citri strains from Argentina, Martinique and Réunion, together with reference copper-resistant Xanthomonas and Stenotrophomonas strains using long-read sequencing technology. Genes involved in copper resistance were found to be strain-dependent with the novel identification in X. citri pv. citri of copABCD and a cus heavy metal efflux resistance-nodulation-division system. The genes providing the adaptive trait were part of a mobile genetic element similar to Tn3-like transposons and included in a conjugative plasmid. This indicates the system's great versatility. The mining of all available bacterial genomes suggested that, within the bacterial community, the spread of copper resistance associated to mobile elements and their plasmid environments was primarily restricted to the Xanthomonadaceae family.

In most phytophagous insects, larvae are less mobile than adults and their fitness depends on the plant chosen by their mother. To maximize fitness, adult preference and larval performance should thus be correlated. This correlation is not always apparent and seems to increase with the level of specialisation, i.e. specialists have a stronger preference for high quality host plant species compared to generalists. The aim of this study was to test whether the relationship between female preference and larval performance was stronger for specialists than for generalists within a community of fruit flies (Diptera: Tephritidae). A total of six fruit fly species was used, including four generalists, and two specialists co-existing in La Reunion island (France). We estimated oviposition preference through the number of eggs laid and larval performance through the larval survival on 29 different host plants species belonging to 15 families in the laboratory and evaluated the relationship between these two traits. Preference-performance relationship differed according to the degree of specialisation with a strong positive correlation for specialists and no relationship for generalists. These results substantiate the theory that choosing high quality hosts is more important for specialists that are adapted to survive on fewer host plants than for generalists.

Background: Phytophagous insects differ in their degree of specialisation on host plants, and range from strictly monophagous species that can develop on only one host plant to extremely polyphagous species that can develop on hundreds of plant species in many families. Nutritional compounds in host fruits affect several larval traits that may be related to adult fitness. In this study, we determined the relationship between fruit nutrient composition and the degree of host specialisation of seven of the eight tephritid species present in La Réunion; these species are known to have very different host ranges in natura. In the laboratory, larval survival, larval developmental time, and pupal weight were assessed on 22 fruit species occurring in La Réunion. In addition, data on fruit nutritional composition were obtained from existing databases. Results: For each tephritid, the three larval traits were significantly affected by fruit species and the effects of fruits on larval traits differed among tephritids. As expected, the polyphagous species Bactrocera zonata, Ceratitis catoirii, C. rosa, and C. capitata were able to survive on a larger range of fruits than the oligophagous species Zeugodacus cucurbitae, Dacus demmerezi, and Neoceratitis cyanescens. Pupal weight was positively correlated with larval survival and was negatively correlated with developmental time for polyphagous species. Canonical correspondence analysis of the relationship between fruit nutrient composition and tephritid survival showed that polyphagous species survived better than oligophagous ones in fruits containing higher concentrations of carbohydrate, fibre, and lipid. Conclusion: Nutrient composition of host fruit at least partly explains the suitability of host fruits for larvae. Completed with female preferences experiments these results will increase our understanding of factors affecting tephritid host range.

Biological invaders have long been hypothesized to exhibit the fast end of the life-history spectrum, with early reproduction and a short lifespan. Here, we examine the rapid evolution of life history within the harlequin ladybird Harmonia axyridis. The species, once used as a biological control agent, is now a worldwide invader. We show that biocontrol populations have evolved a classic fast life history during their maintenance in laboratories. Invasive populations also reproduce earlier than native populations, but later than biocontrol ones. Invaders allocate more resources to reproduction than native and biocontrol individuals, and their reproduction is spread over a longer lifespan. This life history is best described as a bet-hedging strategy. We assert that invasiveness cannot be explained only by invoking faster life histories. Instead, the evolution of life history within invasive populations can progress rapidly and converge to a fine-tuned evolutionary match between the invaded environment and the invader.

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.