Polyphagy is a very common trait among insects. In this study, we focus on a generalist bark-beetle predator, Thanasimus formicarius (L.) (Coleoptera, Cleridae), which feeds on many scolytids in spruce, pine and broad-leaf stands. It is known to respond to the pheromones of many scolytids, among which the most harmful spruce bark beetle in Europe, Ips typographus (L.). The adults attack scolytid adults and oviposit on attacked trees where their larvae feed upon immature stages of the prey. However, a bottom-up process limits Thanasimus formicarius’ impact on spruce bark beetles, because in most cases the bark of spruce is too thin for sheltering pupal niches and mature larvae have to leave the trees. On pine however, pupation is quite successful and reproductive success is high. The present work estimates the advantages (complementary prey during gaps among the phenology of pine bark beetles or due to the population fluctuations of most scolytids) and constraints (landing on unsuitable host trees for the predator’s reproduction) for T. formicarius to have a wide range of prey. Passive barrier-trappings showed that the presence and abundance of scolytid species vary strongly from year to year. So, polyphagy in T. formicarius appears as a response to fluctuating prey supplies. This way of foraging may lead T. formicarius towards stands not always favourable for its development (for example, spruces). At the tree level, funnels and pitfall-traps caught high numbers of third-instar T. formicarius larvae walking on the bark surface of standing spruces infested by Ips typographus (respectively 365 and 70 L3s). After feeding into the whole infested part of the trunk, these larvae are obliged to migrate outside of the galleries to favourable pupation site (e.g. the base of the trees where the bark is thicker), or even to leave the trees and search for an acceptable pupation substrate in the litter. At the landscape level, different trapping experiments showed a correlation between catches of T. formicarius and the proportion of pines around each trap. Consequently, in a metapopulation landscape pattern, pines would act as “sources” of predators, whilst spruces are “sinks”. Indeed, Thanasimus formicarius are trapped in higher numbers in mixed stands comprising pines. This observation is also corroborated in a four-year trapping experiment in the North-East of France, following the storms of December 1999. The predator/prey ratios (T. formicarius/I. typographus) were higher in stands comprising pines than in stands without pines. The first step of a method to estimate Ips typographus infestation trends thanks to the predator/prey ratios was also developed.

Background: The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. Results: We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. Conclusions: The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

Our world is changing rapidly and factors like urbanisation, changed agricultural practices and climate change are causing losses in butterfly diversity. It is therefore of importance to understand the source of their diversity. Given the remarkable diversity of herbivorous insects compared to their non-herbivorous sister groups, changes in host use have been implicated as a promoter of speciation. This thesis looks at geographical aspects of host range evolution and the plasticity of host use. We show that butterflies in the subfamily Nymphalinae that feed on a wide range of host plants have larger geographic ranges than species with narrower host ranges. Although tropical butterflies appear to be more specialised than temperate species, this effect is lost when controlling for the differences in geographic range. Geographic variation in host plant use within Polygonia faunus, related to morphologically distinct subspecies, did not show any genetic differentiation. This suggests that the observed variation in host plant use is a plastic response to environmental differences. Reconstructing host use for the Polygonia-Nymphalis and Vanessa group shows that plasticity is also important for understanding host use at the level of butterfly genera. Using unequal transition costs and including larval feeding ability revealed that frequent colonisations of the same plant genus can often be explained by non-independent processes, such as multiple partial losses of host use, recolonisation of ancestral hosts, and parallel colonisations following a preadaptation for host use. These processes are further reflected in the conservative use of host plant orders within the butterfly family Nymphalidae. Few taxa feed on more than one host plant order, and these expansions occur at the very tips of the tree, which we argue is evidence of the transient nature of generalist host use. These insights improve our understanding of how host range evolution may promote diversification. / At the time of the doctoral defence,the following papers were unpublished and had a status as follows: Paper 3: Submitted; Papers 4 and 5: Manuscripts

Les champignons phytopathogènes sont des parasites majeurs des espèces végétales, autant naturelles que domestiquées. Botrytis cinerea, l’agent de la pourriture grise, en infecte plus de 1400 et est ainsi considéré comme un pathogène généraliste. Pourtant, des données récentes ont mis en évidence une structure des populations liée à leur hôte d’origine. Cette observation soulève l’hypothèse d’une spécialisation à l’hôte, à l’œuvre chez une espèce généraliste. Ce modèle d’étude pourrait permettre de faire avancer la connaissance des mécanismes évolutifs en jeu dans la divergence précoce des populations et la formation de nouvelles espèces fongiques. Cette thèse de doctorat a pour objectifs : (i) de démontrer formellement la spécialisation à l’hôte dans les populations de B. cinerea et d’en déterminer la magnitude et (ii) d’identifier les déterminants génomiques de cette spécialisation. Ainsi j’ai étudié la structure des populations par l’analyse de microsatellites d’un échantillon de 683 isolats, que nous avons corrélé à des tests de pathogénicité croisés sur différents hôtes. Ces travaux ont permis de mettre en évidence la spécialisation de B. cinerea aux hôtes tomate et vigne. En complément de ces lignées sélectionnées, l’espère Botrytis cinerea est constituée d’individus généralistes capables de coloniser les autres hôtes. Des méthodes d’inférence de structure et de généalogies sur des données de polymorphisme issues du séquençage de 32 individus nous ont permis de mieux définir la structure des populations ainsi que d’identifier une lignée spécialisée à la tomate. Enfin, des tests de McDonald-Kreitman et des méthodes de scans génomiques pour détecter des balayages sélectifs ont permis de mettre en évidence des gènes soumis à la sélection divergente entre les populations spécialisées, révélant de possibles déterminants de cette spécialisation. Ces travaux sont ainsi une base pour la validation de plusieurs gènes impliqués dans la pathogénicité hôte-spécifique de B. cinerea, et ouvrent la voie à des améliorations de la gestion du réservoir d’hôtes et des pratiques culturales contre la pourriture grise. / Phytopathogenic fungi are major parasites to wild or domesticated plant species. The grey mold fungus, Botrytis cinerea, infects more than 1400 plant species and thus is considered a broad generalist. However, recent data have revealed population structure correlated to the host of origin of isolates. This observation raises the hypothesis of ongoing host specialization in a generalist species. Studying this question could greatly deepen our theoretical knowledge of the evolutionary mechanisms involved in the early stages of population divergence and subsequent speciation. This thesis aims (i) to formally demonstrate the host specialization in B. cinerea’s populations and determine its magnitude, and (ii) to identify the genomic determinants of this specialization. Thus, I studied population structure based on 683 isolates characterized using microsatellite markers. We compared the inferred genetic structure with variations in aggressiveness measured through cross-pathogenicity tests on multiple hosts. These experiments and analyses confirmed the specialization of B. cinerea to tomato and grapevine hosts. Besides these specialized lineages, the species B. cinerea is composed of generalist individuals capable of infecting multiple hosts. I sequenced the whole genome of 32 individuals and characterized nucleotide polymorphism. Structure inference and genomic genealogy methods allowed us to more accurately define the population structure and identify a lineage specialized on tomato. Lastly, McDonald-Kreitman tests and genomic scans methods allowed the identification of genes under divergent natural selection between populations, revealing possible genomic determinants of specialization. This work can serve as foundation for the validation of multiple genes involved in host-specific pathogenicity of B. cinerea, and pave the way for the implementation of efficient strategies for managing pathogen reservoirs and new agricultural practices for controlling grey mold.

Polyphagy is a very common trait among insects. In this study, we focus on a generalist bark-beetle predator, Thanasimus formicarius (L.) (Coleoptera, Cleridae), which feeds on many scolytids in spruce, pine and broad-leaf stands. It is known to respond to the pheromones of many scolytids, among which the most harmful spruce bark beetle in Europe, Ips typographus (L.). The adults attack scolytid adults and oviposit on attacked trees where their larvae feed upon immature stages of the prey. <p>However, a bottom-up process limits Thanasimus formicarius’ impact on spruce bark beetles, because in most cases the bark of spruce is too thin for sheltering pupal niches and mature larvae have to leave the trees. On pine however, pupation is quite successful and reproductive success is high. <p><p>The present work estimates the advantages (complementary prey during gaps among the phenology of pine bark beetles or due to the population fluctuations of most scolytids) and constraints (landing on unsuitable host trees for the predator’s reproduction) for T. formicarius to have a wide range of prey. <p><p>Passive barrier-trappings showed that the presence and abundance of scolytid species vary strongly from year to year. So, polyphagy in T. formicarius appears as a response to fluctuating prey supplies. <p><p>This way of foraging may lead T. formicarius towards stands not always favourable for its development (for example, spruces). <p>At the tree level, funnels and pitfall-traps caught high numbers of third-instar T. formicarius larvae walking on the bark surface of standing spruces infested by Ips typographus (respectively 365 and 70 L3s). After feeding into the whole infested part of the trunk, these larvae are obliged to migrate outside of the galleries to favourable pupation site (e.g. the base of the trees where the bark is thicker), or even to leave the trees and search for an acceptable pupation substrate in the litter. <p><p>At the landscape level, different trapping experiments showed a correlation between catches of T. formicarius and the proportion of pines around each trap. Consequently, in a metapopulation landscape pattern, pines would act as “sources” of predators, whilst spruces are “sinks”. Indeed, Thanasimus formicarius are trapped in higher numbers in mixed stands comprising pines. This observation is also corroborated in a four-year trapping experiment in the North-East of France, following the storms of December 1999. The predator/prey ratios (T. formicarius/I. typographus) were higher in stands comprising pines than in stands without pines. The first step of a method to estimate Ips typographus infestation trends thanks to the predator/prey ratios was also developed. <p> / Doctorat en sciences, Spécialisation biologie animale / info:eu-repo/semantics/nonPublished