Ecology of Drosophila flies and their microbial symbionts under natural conditions

Les symbioses et le microbiote sont devenus des sujets d’étude prioritaires, souvent explorés grâce à l’organisme modèle Drosophila. Pourtant, nos connaissances des relations naturelles entre drosophiles et symbiotes microbiens, c’est à dire en dehors du laboratoire, sont fragmentaires. Or, comprendre la coévolution entre hôte et symbiotes microbiens nécessite une fine description des effets des partenaires symbiotiques les uns sur les autres. Dans cette thèse, j’ai étudié de façon empirique les interactions entre drosophiles (Drosophila melanogaster et D. suzukii) et symbiotes extracellulaires (bactéries et levures) avec des souches sauvages et dans des conditions qui reproduisaient la nature. Ma thèse a porté sur les trois questions suivantes : (i) comment les drosophiles acquièrent et conservent-elles ces microorganismes tout au long de leur cycle de vie ; (ii) quels sont les effets de ces microorganismes sur le développement de leurs hôtes ; (iii) comment ces microorganismes interagissent-ils entre eux ? Mes travaux ont révélé que levures et bactéries sont plus que des sources de nourriture (i.e. acquisition des ressources) puisqu’elles influencent également comment la larve alloue ses ressources entre traits d’histoire de vie (i.e. plasticité développementale). L’étude des phases d’acquisition et de transmission des symbiotes microbiens par l’insecte en conditions proches de la nature a montré que ceux-ci sont partiellement acquis de l’environnement, conservés entre différents stades de vie, transmis entre générations et lors de l’accouplement. Par ailleurs, j’ai découvert de substantielles interactions entre symbiotes microbiens affectant leur multiplication et leur transmission entre stades de vie de l’hôte. Mon travail révèle une certaine complexité des interactions naturelles entre drosophiles et leurs symbiotes microbiens. Il démontre non seulement que ces interactions sont durables, mais également qu’elles sont composées d’effets imbriqués, simultanés et invisibles dans les systèmes nécessairement simplifiés des laboratoires. Mes travaux apportent également des pistes pour améliorer le contrôle des populations de D. suzukii.Microbiota and symbiotic interactions are priority topics that are often explored using the Drosophila model organism. However, existing knowledge of natural relationships, i.e. in situ, between Drosophila flies and microbial symbionts is fragmented. Understanding coevolution between a host and its microbial symbionts requires a detailed understanding of the co-effects between symbiotic partners. In this PhD, I empirically studied the interactions between Drosophila flies (the model organism D. melanogaster and the pest species D. suzukii) and extracellular microbial symbionts (bacteria and yeasts) using wild strains under near-natural conditions. I investigated three main questions: (i) how do Drosophila flies acquire and transmit their microbial symbionts along their life cycle; (ii) how do these microorganisms affect host development; (iii) how do these microorganisms interact? My work revealed that yeasts and bacteria are not simply sources of nutrition (i.e. resource acquisition) for Drosophila but also influence how fly larva allocate resources between different life history traits (i.e. developmental plasticity). Second, the conducted study on microbial acquisition and transmission phenomena under near-natural conditions showed that symbionts are partially acquired from the environment, conserved through different life stages, and transmitted between generations and through mating. Thirdly, I found substantial interactions between microbial symbionts that affect their multiplication and transmission between host generations. These results reveal natural interactions of some complexity between Drosophila flies and their microbial symbionts. This demonstrates not only that these interactions are durable but also composed of nested effects that are simultaneous and invisible in obligatorily simplified laboratory systems. In addition, this work brings new elements likely to improve population control of the pest D. suzukii

Écologie des drosophiles et de leurs symbiotes microbiens en conditions naturelles

Microbiota and symbiotic interactions are priority topics that are often explored using the Drosophila model organism. However, existing knowledge of natural relationships, i.e. in situ, between Drosophila flies and microbial symbionts is fragmented. Understanding coevolution between a host and its microbial symbionts requires a detailed understanding of the co-effects between symbiotic partners. In this PhD, I empirically studied the interactions between Drosophila flies (the model organism D. melanogaster and the pest species D. suzukii) and extracellular microbial symbionts (bacteria and yeasts) using wild strains under near-natural conditions. I investigated three main questions: (i) how do Drosophila flies acquire and transmit their microbial symbionts along their life cycle; (ii) how do these microorganisms affect host development; (iii) how do these microorganisms interact? My work revealed that yeasts and bacteria are not simply sources of nutrition (i.e. resource acquisition) for Drosophila but also influence how fly larva allocate resources between different life history traits (i.e. developmental plasticity). Second, the conducted study on microbial acquisition and transmission phenomena under near-natural conditions showed that symbionts are partially acquired from the environment, conserved through different life stages, and transmitted between generations and through mating. Thirdly, I found substantial interactions between microbial symbionts that affect their multiplication and transmission between host generations. These results reveal natural interactions of some complexity between Drosophila flies and their microbial symbionts. This demonstrates not only that these interactions are durable but also composed of nested effects that are simultaneous and invisible in obligatorily simplified laboratory systems. In addition, this work brings new elements likely to improve population control of the pest D. suzukii.Les symbioses et le microbiote sont devenus des sujets d’étude prioritaires, souvent explorés grâce à l’organisme modèle Drosophila. Pourtant, nos connaissances des relations naturelles entre drosophiles et symbiotes microbiens, c’est à dire en dehors du laboratoire, sont fragmentaires. Or, comprendre la coévolution entre hôte et symbiotes microbiens nécessite une fine description des effets des partenaires symbiotiques les uns sur les autres. Dans cette thèse, j’ai étudié de façon empirique les interactions entre drosophiles (Drosophila melanogaster et D. suzukii) et symbiotes extracellulaires (bactéries et levures) avec des souches sauvages et dans des conditions qui reproduisaient la nature. Ma thèse a porté sur les trois questions suivantes : (i) comment les drosophiles acquièrent et conservent-elles ces microorganismes tout au long de leur cycle de vie ; (ii) quels sont les effets de ces microorganismes sur le développement de leurs hôtes ; (iii) comment ces microorganismes interagissent-ils entre eux ? Mes travaux ont révélé que levures et bactéries sont plus que des sources de nourriture (i.e. acquisition des ressources) puisqu’elles influencent également comment la larve alloue ses ressources entre traits d’histoire de vie (i.e. plasticité développementale). L’étude des phases d’acquisition et de transmission des symbiotes microbiens par l’insecte en conditions proches de la nature a montré que ceux-ci sont partiellement acquis de l’environnement, conservés entre différents stades de vie, transmis entre générations et lors de l’accouplement. Par ailleurs, j’ai découvert de substantielles interactions entre symbiotes microbiens affectant leur multiplication et leur transmission entre stades de vie de l’hôte. Mon travail révèle une certaine complexité des interactions naturelles entre drosophiles et leurs symbiotes microbiens. Il démontre non seulement que ces interactions sont durables, mais également qu’elles sont composées d’effets imbriqués, simultanés et invisibles dans les systèmes nécessairement simplifiés des laboratoires. Mes travaux apportent également des pistes pour améliorer le contrôle des populations de D. suzukii

Écologie des drosophiles et de leurs symbiotes microbiens en conditions naturelles

Microbiota and symbiotic interactions are priority topics that are often explored using the Drosophila model organism. However, existing knowledge of natural relationships, i.e. in situ, between Drosophila flies and microbial symbionts is fragmented. Understanding coevolution between a host and its microbial symbionts requires a detailed understanding of the co-effects between symbiotic partners. In this PhD, I empirically studied the interactions between Drosophila flies (the model organism D. melanogaster and the pest species D. suzukii) and extracellular microbial symbionts (bacteria and yeasts) using wild strains under near-natural conditions. I investigated three main questions: (i) how do Drosophila flies acquire and transmit their microbial symbionts along their life cycle; (ii) how do these microorganisms affect host development; (iii) how do these microorganisms interact? My work revealed that yeasts and bacteria are not simply sources of nutrition (i.e. resource acquisition) for Drosophila but also influence how fly larva allocate resources between different life history traits (i.e. developmental plasticity). Second, the conducted study on microbial acquisition and transmission phenomena under near-natural conditions showed that symbionts are partially acquired from the environment, conserved through different life stages, and transmitted between generations and through mating. Thirdly, I found substantial interactions between microbial symbionts that affect their multiplication and transmission between host generations. These results reveal natural interactions of some complexity between Drosophila flies and their microbial symbionts. This demonstrates not only that these interactions are durable but also composed of nested effects that are simultaneous and invisible in obligatorily simplified laboratory systems. In addition, this work brings new elements likely to improve population control of the pest D. suzukii.Les symbioses et le microbiote sont devenus des sujets d’étude prioritaires, souvent explorés grâce à l’organisme modèle Drosophila. Pourtant, nos connaissances des relations naturelles entre drosophiles et symbiotes microbiens, c’est à dire en dehors du laboratoire, sont fragmentaires. Or, comprendre la coévolution entre hôte et symbiotes microbiens nécessite une fine description des effets des partenaires symbiotiques les uns sur les autres. Dans cette thèse, j’ai étudié de façon empirique les interactions entre drosophiles (Drosophila melanogaster et D. suzukii) et symbiotes extracellulaires (bactéries et levures) avec des souches sauvages et dans des conditions qui reproduisaient la nature. Ma thèse a porté sur les trois questions suivantes : (i) comment les drosophiles acquièrent et conservent-elles ces microorganismes tout au long de leur cycle de vie ; (ii) quels sont les effets de ces microorganismes sur le développement de leurs hôtes ; (iii) comment ces microorganismes interagissent-ils entre eux ? Mes travaux ont révélé que levures et bactéries sont plus que des sources de nourriture (i.e. acquisition des ressources) puisqu’elles influencent également comment la larve alloue ses ressources entre traits d’histoire de vie (i.e. plasticité développementale). L’étude des phases d’acquisition et de transmission des symbiotes microbiens par l’insecte en conditions proches de la nature a montré que ceux-ci sont partiellement acquis de l’environnement, conservés entre différents stades de vie, transmis entre générations et lors de l’accouplement. Par ailleurs, j’ai découvert de substantielles interactions entre symbiotes microbiens affectant leur multiplication et leur transmission entre stades de vie de l’hôte. Mon travail révèle une certaine complexité des interactions naturelles entre drosophiles et leurs symbiotes microbiens. Il démontre non seulement que ces interactions sont durables, mais également qu’elles sont composées d’effets imbriqués, simultanés et invisibles dans les systèmes nécessairement simplifiés des laboratoires. Mes travaux apportent également des pistes pour améliorer le contrôle des populations de D. suzukii

Écologie des drosophiles et de leurs symbiotes microbiens en conditions naturelles

Microbiota and symbiotic interactions are priority topics that are often explored using the Drosophila model organism. However, existing knowledge of natural relationships, i.e. in situ, between Drosophila flies and microbial symbionts is fragmented. Understanding coevolution between a host and its microbial symbionts requires a detailed understanding of the co-effects between symbiotic partners. In this PhD, I empirically studied the interactions between Drosophila flies (the model organism D. melanogaster and the pest species D. suzukii) and extracellular microbial symbionts (bacteria and yeasts) using wild strains under near-natural conditions. I investigated three main questions: (i) how do Drosophila flies acquire and transmit their microbial symbionts along their life cycle; (ii) how do these microorganisms affect host development; (iii) how do these microorganisms interact? My work revealed that yeasts and bacteria are not simply sources of nutrition (i.e. resource acquisition) for Drosophila but also influence how fly larva allocate resources between different life history traits (i.e. developmental plasticity). Second, the conducted study on microbial acquisition and transmission phenomena under near-natural conditions showed that symbionts are partially acquired from the environment, conserved through different life stages, and transmitted between generations and through mating. Thirdly, I found substantial interactions between microbial symbionts that affect their multiplication and transmission between host generations. These results reveal natural interactions of some complexity between Drosophila flies and their microbial symbionts. This demonstrates not only that these interactions are durable but also composed of nested effects that are simultaneous and invisible in obligatorily simplified laboratory systems. In addition, this work brings new elements likely to improve population control of the pest D. suzukii.Les symbioses et le microbiote sont devenus des sujets d’étude prioritaires, souvent explorés grâce à l’organisme modèle Drosophila. Pourtant, nos connaissances des relations naturelles entre drosophiles et symbiotes microbiens, c’est à dire en dehors du laboratoire, sont fragmentaires. Or, comprendre la coévolution entre hôte et symbiotes microbiens nécessite une fine description des effets des partenaires symbiotiques les uns sur les autres. Dans cette thèse, j’ai étudié de façon empirique les interactions entre drosophiles (Drosophila melanogaster et D. suzukii) et symbiotes extracellulaires (bactéries et levures) avec des souches sauvages et dans des conditions qui reproduisaient la nature. Ma thèse a porté sur les trois questions suivantes : (i) comment les drosophiles acquièrent et conservent-elles ces microorganismes tout au long de leur cycle de vie ; (ii) quels sont les effets de ces microorganismes sur le développement de leurs hôtes ; (iii) comment ces microorganismes interagissent-ils entre eux ? Mes travaux ont révélé que levures et bactéries sont plus que des sources de nourriture (i.e. acquisition des ressources) puisqu’elles influencent également comment la larve alloue ses ressources entre traits d’histoire de vie (i.e. plasticité développementale). L’étude des phases d’acquisition et de transmission des symbiotes microbiens par l’insecte en conditions proches de la nature a montré que ceux-ci sont partiellement acquis de l’environnement, conservés entre différents stades de vie, transmis entre générations et lors de l’accouplement. Par ailleurs, j’ai découvert de substantielles interactions entre symbiotes microbiens affectant leur multiplication et leur transmission entre stades de vie de l’hôte. Mon travail révèle une certaine complexité des interactions naturelles entre drosophiles et leurs symbiotes microbiens. Il démontre non seulement que ces interactions sont durables, mais également qu’elles sont composées d’effets imbriqués, simultanés et invisibles dans les systèmes nécessairement simplifiés des laboratoires. Mes travaux apportent également des pistes pour améliorer le contrôle des populations de D. suzukii

How to disentangle symbiont effects on host resource acquisition and plasticity, and why it matters for their evolution

National audienceMicrobial symbionts can either provide resources to their hosts or mediate host plasticity through physiological signaling. Symbionts that improve resource availability would be beneficial in all environments, which favors the evolution of stable mutualism. However, when symbiont affects plasticity, fitness consequences would depend on the environmental context, with consequences on coevolution. In order to separate symbiont effects on host resources and plasticity, we propose a new multivariate framework based on the analysis of trade-offs between fitness components. We applied the framework to a series of experiments on the symbiosis between bacteria, yeasts and three fruit-fly species, Drosophila melanogaster, D. simulans and D. suzukii. In particular, we focused on the trade-off between speed of larval development and adult size that is largely documented in holometabolous insects. We found evidence for symbiont effects on both host resources availability and developmental plasticity. Taking into account host sex, genotype and species revealed a major effect of host species on whether yeast affects plasticity or not. Besides, evidence suggests Drosophila's bacterial symbionts may influence plasticity more than yeast does. Further developments of the framework will enable the simultaneous analysis of a greater number of fitness components and should encompass other types of variation (e.g. genetic). Until our framework's evolutionary predictions are tested, its results can be used to improve the mass-production of insect (e.g. for the sterile insect technique) so as to fine-tune insect vigor and phenotype to contextual need

Floral Scent and Pollinators of Cypripedium calceolus L. at Different Latitudes

International audienceFloral scent is an important trait in plant–pollinator interactions. It not only varies among plant species but also among populations within species. Such variability might be caused by various non–selective factors, or, as has been shown in some instances, might be the result of divergent selective pressures exerted by variable pollinator climates. Cypripedium calceolus is a Eurasian deceptive orchid pollinated mainly by bees, which spans wide altitudinal and latitudinal gradients in mainly quite isolated populations. In the present study, we investigated whether pollinators and floral scents vary among different latitudes. Floral scents of three C. calceolus populations in the Southern Alps were collected by dynamic headspace and analyzed by gas chromatography coupled to mass spectrometry (GC/MS). These data were completed by previously published scent data of the Northern Alps and Scandinavia. The scent characteristics were compared with information on pollinators recorded for present study or available in the literature. More than 80 scent compounds were overall recorded from plants of the three regions, mainly aliphatics, terpenoids, and aromatics. Seven compounds were found in all samples, and most samples were dominated by linalool and octyl acetate. Although scents differed among regions and populations, the main compounds were similar among regions. Andrena and Lasioglossum species were the main pollinators in all three regions, with Andrena being relatively more abundant than Lasioglossum in Scandinavia. We discuss natural selection mediated by pollinators and negative frequency–dependent selection as possible reasons for the identified variation of floral scent within and among populations and regions

The partitioning of symbionts effects on host resource acquisition and developmental plasticity

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

Yeast facilitates the multiplication of Drosophila bacterial symbionts but has no effect on the form or parameters of Taylor’s law

International audienceInteractions 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 in Drosophila 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 with D. melanogaster larvae 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 of D. melanogaster's symbiosis with yeast and bacteria. They further reveal the complexity of investigating TL with microorganisms

Deciphering symbiont effects on host plasticity and ressource acquisition in Drosophila species

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Yeast facilitates the multiplication of <i>Drosophila</i> bacterial symbionts but has no effect on the form or parameters of Taylor’s law

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 in Drosophila 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 with D. melanogaster larvae 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 of D. melanogaster’s symbiosis with yeast and bacteria. They further reveal the complexity of investigating TL with microorganisms.</p