@article{KaechDennisVorburger2021,
  author    = {Kaech, Heidi and Dennis, Alice B. and Vorburger, Christoph},
  title     = {Triple RNA-Seq characterizes aphid gene expression in response to infection with unequally virulent strains of the endosymbiont Hamiltonella defensa},
  series = {BMC genomics},
  volume    = {22},
  journal   = {BMC genomics},
  number    = {1},
  publisher = {BioMed Central},
  address   = {London},
  issn      = {1471-2164},
  doi       = {10.1186/s12864-021-07742-8},
  pages     = {21},
  year      = {2021},
  abstract  = {Background Secondary endosymbionts of aphids provide benefits to their hosts, but also impose costs such as reduced lifespan and reproductive output. The aphid Aphis fabae is host to different strains of the secondary endosymbiont Hamiltonella defensa, which encode different putative toxins. These strains have very different phenotypes: They reach different densities in the host, and the costs and benefits (protection against parasitoid wasps) they confer to the host vary strongly. Results We used RNA-Seq to generate hypotheses on why four of these strains inflict such different costs to A. fabae. We found different H. defensa strains to cause strain-specific changes in aphid gene expression, but little effect of H. defensa on gene expression of the primary endosymbiont, Buchnera aphidicola. The highly costly and over-replicating H. defensa strain H85 was associated with strongly reduced aphid expression of hemocytin, a marker of hemocytes in Drosophila. The closely related strain H15 was associated with downregulation of ubiquitin-related modifier 1, which is related to nutrient-sensing and oxidative stress in other organisms. Strain H402 was associated with strong differential regulation of a set of hypothetical proteins, the majority of which were only differentially regulated in presence of H402. Conclusions Overall, our results suggest that costs of different strains of H. defensa are likely caused by different mechanisms, and that these costs are imposed by interacting with the host rather than the host's obligatory endosymbiont B. aphidicola.},
  language  = {en}
}
@article{DennisBallesterosRobinetal.2020,
  author    = {Dennis, Alice B. and Ballesteros, Gabriel I. and Robin, St{\´e}phanie and Schrader, Lukas and Bast, Jens and Bergh{\"o}fer, Jan and Beukeboom, Leo W. and Belghazi, Maya and Bretaudeau, Anthony and Buellesbach, Jan and Cash, Elizabeth and Colinet, Dominique and Dumas, Zo{\´e} and Errbii, Mohammed and Falabella, Patrizia and Gatti, Jean-Luc and Geuverink, Elzemiek and Gibson, Joshua D. and Hertaeg, Corinne and Hartmann, Stefanie and Jacquin-Joly, Emmanuelle and Lammers, Mark and Lavandero, Blas I. and Lindenbaum, Ina and Massardier-Galata, Lauriane and Meslin, Camille and Montagn{\´e}, Nicolas and Pak, Nina and Poiri{\´e}, Maryl{\`e}ne and Salvia, Rosanna and Smith, Chris R. and Tagu, Denis and Tares, Sophie and Vogel, Heiko and Schwander, Tanja and Simon, Jean-Christophe and Figueroa, Christian C. and Vorburger, Christoph and Legeai, Fabrice and Gadau, J{\"u}rgen},
  title     = {Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum},
  series = {BMC Genomics},
  volume    = {21},
  journal   = {BMC Genomics},
  publisher = {BioMed Central},
  address   = {London},
  issn      = {1471-2164},
  doi       = {10.1186/s12864-020-6764-0},
  pages     = {27},
  year      = {2020},
  abstract  = {Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. Results We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8\%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes. Conclusions These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.},
  language  = {en}
}
@misc{DennisBallesterosRobinetal.2020,
  author    = {Dennis, Alice B. and Ballesteros, Gabriel I. and Robin, St{\´e}phanie and Schrader, Lukas and Bast, Jens and Bergh{\"o}fer, Jan and Beukeboom, Leo W. and Belghazi, Maya and Bretaudeau, Anthony and Buellesbach, Jan and Cash, Elizabeth and Colinet, Dominique and Dumas, Zo{\´e} and Errbii, Mohammed and Falabella, Patrizia and Gatti, Jean-Luc and Geuverink, Elzemiek and Gibson, Joshua D. and Hertaeg, Corinne and Hartmann, Stefanie and Jacquin-Joly, Emmanuelle and Lammers, Mark and Lavandero, Blas I. and Lindenbaum, Ina and Massardier-Galata, Lauriane and Meslin, Camille and Montagn{\´e}, Nicolas and Pak, Nina and Poiri{\´e}, Maryl{\`e}ne and Salvia, Rosanna and Smith, Chris R. and Tagu, Denis and Tares, Sophie and Vogel, Heiko and Schwander, Tanja and Simon, Jean-Christophe and Figueroa, Christian C. and Vorburger, Christoph and Legeai, Fabrice and Gadau, J{\"u}rgen},
  title     = {Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  number    = {989},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-47612},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-476129},
  pages     = {29},
  year      = {2020},
  abstract  = {Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. Results We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8\%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes. Conclusions These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.},
  language  = {en}
}
@article{MattheyDoretvanderKooiJeffriesetal.2019,
  author    = {Matthey-Doret, Cyril and van der Kooi, Casper J. and Jeffries, Daniel L. and Bast, Jens and Dennis, Alice B. and Vorburger, Christoph and Schwander, Tanja},
  title     = {Mapping of Multiple Complementary Sex Determination Loci in a Parasitoid Wasp},
  series = {Genome biology and evolution},
  volume    = {11},
  journal   = {Genome biology and evolution},
  number    = {10},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {1759-6653},
  doi       = {10.1093/gbe/evz219},
  pages     = {2954 -- 2962},
  year      = {2019},
  abstract  = {Sex determination has evolved in a variety of ways and can depend on environmental and genetic signals. A widespread form of genetic sex determination is haplodiploidy, where unfertilized, haploid eggs develop into males and fertilized diploid eggs into females. One of the molecular mechanisms underlying haplodiploidy in Hymenoptera, the large insect order comprising ants, bees, and wasps, is complementary sex determination (CSD). In species with CSD, heterozygosity at one or several loci induces female development. Here, we identify the genomic regions putatively underlying multilocus CSD in the parasitoid wasp Lysiphlebus fabarum using restriction -site associated DNA sequencing. By analyzing segregation patterns at polymorphic sites among 331 diploid males and females, we identify up to four CSD candidate regions, all on different chromosomes. None of the candidate regions feature evidence for homology with the csd gene from the honey bee, the only species in which CSD has been characterized, suggesting that CSD in L. fabarum is regulated via a novel molecular mechanism. Moreover, no homology is shared between the candidate loci, in contrast to the idea that multilocus CSD should emerge from duplications of an ancestral single -locus system. Taken together, our results suggest that the molecular mechanisms underlying CSD in Hymenoptera are not conserved between species, raising the question as to whether CSD may have evolved multiple times independently in the group.},
  language  = {en}
}
@article{KaechMatheHubertDennisetal.2018,
  author    = {K{\"a}ch, Heidi and Mathe-Hubert, Hugo and Dennis, Alice B. and Vorburger, Christoph},
  title     = {Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids},
  series = {Evolutionary applications},
  volume    = {11},
  journal   = {Evolutionary applications},
  number    = {2},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {1752-4571},
  doi       = {10.1111/eva.12532},
  pages     = {220 -- 230},
  year      = {2018},
  abstract  = {There is growing interest in biological control as a sustainable and environmentally friendly way to control pest insects. Aphids are among the most detrimental agricultural pests worldwide, and parasitoid wasps are frequently employed for their control. The use of asexual parasitoids may improve the effectiveness of biological control because only females kill hosts and because asexual populations have a higher growth rate than sexuals. However, asexuals may have a reduced capacity to track evolutionary change in their host populations. We used a factorial experiment to compare the ability of sexual and asexual populations of the parasitoid Lysiphlebus fabarum to control caged populations of black bean aphids (Aphis fabae) of high and low clonal diversity. The aphids came from a natural population, and one-third of the aphid clones harbored Hamiltonella defensa, a heritable bacterial endosymbiont that increases resistance to parasitoids. We followed aphid and parasitoid population dynamics for 3months but found no evidence that the reproductive mode of parasitoids affected their effectiveness as biocontrol agents, independent of host clonal diversity. Parasitoids failed to control aphids in most cases, because their introduction resulted in strong selection for clones protected by H.defensa. The increasingly resistant aphid populations escaped control by parasitoids, and we even observed parasitoid extinctions in many cages. The rapid evolution of symbiont-conferred resistance in turn imposed selection on parasitoids. In cages where asexual parasitoids persisted until the end of the experiment, they became dominated by a single genotype able to overcome the protection provided by H.defensa. Thus, there was evidence for parasitoid counteradaptation, but it was generally too slow for parasitoids to regain control over aphid populations. It appears that when pest aphids possess defensive symbionts, the presence of parasitoid genotypes able to overcome symbiont-conferred resistance is more important for biocontrol success than their reproductive mode.},
  language  = {en}
}
@article{DennisPatelOliveretal.2017,
  author    = {Dennis, Alice B. and Patel, Vilas and Oliver, Kerry M. and Vorburger, Christoph},
  title     = {Parasitoid gene expression changes after adaptation to symbiont-protected hosts},
  series = {Evolution},
  volume    = {71},
  journal   = {Evolution},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0014-3820},
  doi       = {10.1111/evo.13333},
  pages     = {2599 -- 2617},
  year      = {2017},
  abstract  = {Reciprocal selection between aphids, their protective endosymbionts, and the parasitoid wasps that prey upon them offers an opportunity to study the basis of their coevolution. We investigated adaptation to symbiont\&\#8208;conferred defense by rearing the parasitoid wasp Lysiphlebus fabarum on aphids (Aphis fabae) possessing different defensive symbiont strains (Hamiltonella defensa). After ten generations of experimental evolution, wasps showed increased abilities to parasitize aphids possessing the H. defensa strain they evolved with, but not aphids possessing the other strain. We show that the two symbiont strains encode different toxins, potentially creating different targets for counter\&\#8208;adaptation. Phenotypic and behavioral comparisons suggest that neither life\&\#8208;history traits nor oviposition behavior differed among evolved parasitoid lineages. In contrast, comparative transcriptomics of adult female wasps identified a suite of differentially expressed genes among lineages, even when reared in a common, symbiont\&\#8208;free, aphid host. In concurrence with the specificity of each parasitoid lineages' infectivity, most differentially expressed parasitoid transcripts were also lineage\&\#8208;specific. These transcripts are enriched with putative venom toxins and contain highly expressed, potentially defensive viral particles. Together, these results suggest that wild populations of L. fabarum employ a complicated offensive arsenal with sufficient genetic variation for wasps to adapt rapidly and specifically to their hosts' microbial defenses.},
  language  = {en}
}